Insect crop pests and the changing climate

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Insect crop pests and the changing climate*

Richard Harrington and Ian P. Woiwod Rothamsted Experimental Station, Harpenden, Hertfordshire

Following the recent run of mild winters, there have been numerous reports of certain insects appearing earlier and in larger numbers than usual, and even of the occasional exotic insect turning up on our shores. The media have been quick to follow up the more alarmist aspects of these reports and have often come to the Rothamsted Experimental Station for information, as we operate a nationwide network of suction traps for monitoring aphids, and light traps for monitoring moths. Traps are emptied daily and the aphids and moths identi- fied to species. As some of the suction traps

* This article is adapted from a report written for Greenpeace Ltd.

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have been run for 30 years and some of the moth traps for even longer, we have at our disposal a unique source of standardised data with which long-term trends and short-term anomalies in insect distribution, abundance, and timing can be detected. Here, we describe the potential effects of climate on insect abundance and distribution, explain some interactions with other factors which may occur, and give examples of what has happened to aphids and moths after mild winters.

The potential effects of climate on insect populations

The importance of climate and weather events for the distribution of insects and their popula-

tion dynamics has long been appreciated, particularly in applied studies on pest species. A review of the subject was published by Uvarov (1931) and, even then, he referred to over 1150 relevant papers and books. Today, the explo- sion of entomological literature would make a complete review impossible, but the proceed- ings of the recent symposium of the Royal Entomological Society (Harrington and Stork 1995) includes many relevant contributions, and the reviews of Porter et al. (1991) and Cammell and Knight (1992) also provide excel- lent summaries on which this article draws.

The possible effects of a changing climate can be divided into eight main categories.

(i) Change in geographical distribution. This is usually considered in the context of the invasion of new pest species, but invasion by predators and parasites may also occur and be beneficial for pest control. As the species rich- ness of insects tends to increase with temperature (Turner et al. 1987), the prediction is that as temperature rises more species will be gained than lost and some of these species will be pests. This is particularly likely because pests are often very mobile species, able to respond rapidly to a fluctuating or changing climate. However, known pest species may not be pests if introduced into a new environment; conditions may be marginal for their survival, or suitable crop hosts may be absent. A simple calculation predicts that a 1 degC temperature rise in the UK would enable a species to spread 200km northwards or 140m upwards in alti- tude (Parry et al. 1989).

(ii) Increased risk of invasion. Some important pests are long-range migrants and move into crops in areas where they cannot overwinter successfully. It has been suggested that invasion by such long-range migrants may become more frequent if the ranges of these species extend further north into continental Europe (Porter et al. 1991).

(iii) Changes in overwintering success. Mild winters are likely to increase the overwintering survival of insects. However, this may not be true if predators, parasites and diseases are also favoured or if hibernation (overwintering dis- pause) is disrupted.

(iv) Changes in interactions between species. These could be interactions with competitors

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or natural enemies. Such changes may increase or decrease pest problems as different species respond differentially to climatic change.

(v) Changes in population growth rate. Rates of change in population growth are affected through changes in survival, development, reproduction and movement, all of which are temperature-dependent.

(vi) Increases in the number of generations per year. Species differ in their flexibility in this respect. Some species such as aphids fit in as many generations per year as temperature and food-plant quality allow, whereas other species are adapted to a single generation and any speeding-up of generation time has to be com- pensated for by longer periods of dormancy, often as hibernation or aestivation. It is generally considered that the more generations per year there are, the greater the possibility of damaging populations.

(vii) Extension of the development season. This might also lead to an increase in the number of generations, but might also allow time for natural enemies to respond to pest population increases. Some species may be limited in their ability to respond to longer seasons by their adaption to day length.

(viii) Changes in crop-pest synchrony. The pest status of insects is often related to the growth stage of their host plants. Climate change may disrupt this relationship although there is evidence that adaptation can take place over time. The effect of changes in synchrony is considered to be particularly important for forest pests, notably moths, which are adapted to feed on newly emerged foliage in spring (Dewar and Watt 1992).

In addition to the natural effects listed above, any change in climatic variables will alter the range of exotic pests that could survive and multiply in the UK after accidental or deliber- ate introduction. Much research has been done on this subject internationally to underpin quarantine requirements designed to keep out potential pests, and to support the development of biological control programmes where the interest is often in importing exotic parasites to control accidentally introduced pests. For example, at the moment, only species able to survive in temperate regions of the world such as New Zealand or northern Europe are

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likely to pose a threat to the UK. However, an increase in average temperature, particularly in winter, is likely to enable a wider range of species to pose a threat.

Published work can provide examples to support most of the theoretical effects listed above. However, as so many interactions between meteorological factors, pests, their host plants, and their natural enemies are possible (Fig. l), and there are over 20000 insect species in the British Isles alone, the task of predicting accurately the effect of any particular climate change scenario on the general insect fauna is impossible. However, using data from the spatially and temporally extensive trap networks of the Rothamsted Insect Survey we are able to report on the responses of moths and aphids to fluctuating weather, the extremes of which (especially high temperature extremes) are expected to be the norms in the future, and hence we can begin to predict likely changes in these insect populations with changes in climate.

Aphids and climate change

In Britain, aphids are the most important group of agricultural pests as they have a high repro-

ductive rate, cause direct feeding damage, and are efficient vectors of plant virus diseases. Among over 500 British aphid species there are important pests of arable, forest and horticultural crops, and some species are well known as garden pests on vegetable and orna- mental plants. They are parthenogenetic for some or all of the year, giving birth to active young (rather than eggs) without the need to mate. As soon as an aphid becomes adult, which may take as little as a week from birth, it is almost ready to give birth, and the following generation is already present within the oldest embryos. Some species have a sexual phase in autumn which leads to a cold hardy egg suitable for surviving the severest British winters. However, unlike the eggs, active forms from the year-round parthenogenetic species can take advantage of mild winters with continued development and reproduction. There is, hence, a trade-off between the risk of death and the potential for increase when contrasting the possible effects on aphids that pass the winter as an egg or as an active individual. In species where both strategies are possible, active forms tend to predominate in areas where winters are mild; the extent of these areas may increase in the future.

Natural enemies 4

Fig. 1 change (fonz Hurnngton and Stork 1995)

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IriterumoiiA bctweeii ubioiic und bzotzc factors tliat w e d to be undmtood zri order to predzct the eflects of clznzate

Another important feature of aphid biology is their mobility. Adults of most species have winged as well as wingless forms. The winged forms are produced in response to overcrowd- ing, to a reduction in plant quality, or to changes in day length that indicate the time to move between alternate host plants. They are wind-borne migrants, able to move long dis- tances, although the majority of flights are probably within a few kilometres. It is these winged aphids that are monitored by the suction traps.

One of the many uses of the suction trap data has been to develop forecasting systems so that control measures are taken only when the pest is likely to be a problem, thereby improving control and preventing unnecessary precau- tionary spraying. Since temperature influences nearly all aspects of aphid biology, many of these forecasts are based on climatic variables such as mean temperature and can therefore be adapted almost immediately to provide predictions of the effect of climate change on aphid dynamics. In several species which do not overwinter as eggs, there is a strong statistical relationship between winter temperature and the earliness of flight or abundance in spring

Q 2 +-

(Harrington et al. 1990). Such simple statistical relationships have been found to provide many of the most useful forecasts. Also, the com- monly used climate change scenarios for Bri- tain have mean winter temperatures that lie within the range used to develop the models. We can, therefore, be fairly confident of predictions derived from them, with the proviso that long periods of milder winter weather may enable natural enemies to exert greater control of pest populations.

The climate change forecasts for the important virus vector Myzus persicae (the peach potato aphid) suggest that an increase in mean temperature in January and February of 1 degC advances the time of the spring migration by about two weeks (Fig. 2). The timing of the spring migration into field crops is important for virus transmission and any such advance will increase virus problems. This prediction has been examined and shown to be valid across a range of 14 degrees of latitude in Europe (Harrington et al. 1992). The other climate change forecast for M. persicae predicts that the number of migrants in suction-trap catches, up to the end of June, will increase. This is a measure of the population multiplica-

0 0

b r i l 7

3.3% Average..

1988-1894

Jan - Feb mean screen temperature Fig. 2 The relationship between annual date of first appearance of Myzus persicae in the Rothamsted suction trap against mean temperature inJanuary and February 1968 to 1994. The mean for the period and the prediction for 2050 are shown.

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tion in spring and is likely to relate to the pest status of the species in any particular year. Compar- ing the January-February mean temperature at Rothamsted between 1968 and 1994 (3.3"C) with that predicted for 2050 (6.2"C) by the De- partment of the Environment (1991), the numbers in the trap are forecast to increase 15 times, although this prediction has yet to be validated for other sites. Most clones ofM. persicae are parthenogenetic throughout the year. Based on mean accumulated temperatures at Rothamsted between 1966 and 1990 such aphids would complete 18 generations in an average year. However, with warming of an average of 2 degC this would increase to apredicted 23 generations.

In our opinion these aphid predictions are some of the most reliable because they are based on long runs of field data using the natural annual variation in UIC climate and robust statistical methods which implicitly in- clude the effects of many factors. Aphid problems in the UIC will probably increase under most existing climate change scenarios; this conclusion is strengthened by observations made during recent warm years, which are described later.

Moths and climate change

The Lepidoptera (butterflies and moths) is an insect order that contains some of the world's most important pests. Although Carter (1984) lists 200 British species known to be pests throughout Europe, with one or two exceptions representatives in the groups are only spo- radically important in Britain. The three ob- vious exceptions are the pea moth, C-ydia nigricuncl, the codling moth, C y f i a porrionelh, and the large white butterfly, Pieris brassicae, all of which are important horticultural and garden pests. There are also a number of regular forest pest moths, perhaps the best known being the pine beauty, Panolis flaiiim~ti, which has recently caused heavy damage to non-native pine plantations in Scotland (Watt and Leather 1988). Another important group are the larvae of several noctuid moth species which are known collectively as cutworms because of their habit of eating crop plants at ground level. These can be pests in Britain, but

only occasionally and in localised areas. One moth species, the European corn borer,

Ostrinia nubilalis, has been used in one of the few attempts to predict the possible range extension of a species in Europe as a result of expected climate change. This species is of agricultural importance over much of the Northern Hemisphere between the latitudes of 10 and 58"N in Europe, Asia, northern Africa and America, and is a pest of all types of maize. Currently in the UK it is a rare species found around London and on the south coast near Southampton, feeding on mugwort. Using a best-case (0-1.5degC rise by 2020) and worst- case (1.5-2.5degC rise by 2020) scenario Por- ter (1995) estimated that the species might move northwards at a rate of between zero and 350km per decade depending on the region and extent of warming. At present this would not cause a great problem in the UK as very little grain maize is grown. However, if temperatures rise, more of Britain would become suitable for this crop, and this potential can be predicted using the same methods. It was also calculated that by 2050, under the most extreme warming expected, an extra generation could occur in many regions where the moth is already present, further increasing the pest potential of the species, although artificial and natural control would also change, thereby making predictions uncertain.

There are other examples of the effects of temperature rise on UIC moths. It has been shown that the number of eggs laid by the pine beauty moth increases with temperature (Watt and Leather 1988). The partial second generation of the codling moth in Britain map become much more important than at present for this garden and horticultural pest (M. E. Solomon, personal communication). Generally, as moths are more important as agricultural pests further south in Europe the presumption is that future temperature rises are likely to lead to new or increased problems with this important group within the UIC. However, changes in insect- plant synchrony may actually lead to decreased pest status, for example in the winter moth, Operophreru brmmuta, a well known horticultural and garden pest on fruit trees (Dewar and Watt 1992). The situation will need to be carefully monitored.

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Other insect pests

Very little has been published directly on climate change and pests belonging to insect groups other than aphids or moths. A notable exception is that of the cabbage root fly, Delia radicum (Collier et al. 1991), a serious pest of cruciferous crops. This analysis was based on detailed simulation modelling done to provide information on cabbage root fly populations. From this model it was estimated that a 3 degC increase in mean daily temperature would cause this species to become active about a month earlier than at present, but the present three generations per year would not increase to four without temperature increases between 5 and 10degC.

One other climate change analysis may have significance for UK agriculture. The CLIMEX programme was used to predict the number of generations of the Colorado beetle that would be possible under our present climate com- pared with that of the future. This analysis showed that such an increase would lead to at least one extra generation throughout most of Britain (Sutherst et al. 1995). The Colorado beetle is not a resident species in Britain at the

moment and is kept out by very stringent quarantine regulations because its introduction could severely damage the UK potato crop. However, populations in neighbouring areas on the European mainland may be larger in the future, reducing the possibility of excluding this species from Britain.

Insect conservation

Although the emphasis of this article is on insects which are potential or actual crop pests these form only a very small proportion of the total species pool, and changes in populations of non-pest species may have important conservation implications. Most of the interest in this respect has been directed towards the likely effect of climate change on the butterflies as it is this group which is thought to be particularly sensitive to temperature and also, unlike most insect groups, has a high and positive public profile. A very full consideration of all aspects of butterfly ecology and climate has recently been published in Dennis (1993) who indicates just how complex and subtle such relationships can be.

If the general trend is for insects from many

Cumulus and pack ice

CT 0 Jeremy P. Thomas Cumulus above open pack ice in the Weddell Sea on 6 December 1991

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species to become commoner as mean temperatures rise and winters become milder then, unlike agricultural entomologists, insect con- servationists might have little to be concerned about. However, things may not be that simple. Many of the rarer species in Britain are at the edge of their range here and are thus concen- trated in the south and often confined to particularly warm microhabitats such as south- facing slopes of chalk grassland (e.g. the adonis blue, Lysandru bellurgus) or early successional stages in coppiced woodland (cg. the fritillaries). It is these species particularly among the butterflies that have decreased so markedly in Britain over the last 50 years, often as a result of subtle changes in habitat quality as much as habitat destruction. Thus the fritillaries have almost completely disappeared from eastern England although the woods they formerly inhabited still remain (Woiwod and Thomas 1993). Warmer conditions should favour these species and enable them to survive further north, and also to be less fussy about their habitat requirements. Unfortunately, the landscape has become very fragmented due to urban development and agricultural intensifica- tion and there may be real problems in rare or local species finding the few small patches of suitable areas for breeding even if the numbers of these increase under climate change.

Perhaps of even more concern are those species that colonised Britain as the last ice age receded, approximately 10 000 years ago. The southern limit of their range in Britain is likely to be in the north, and often they are only to be found at higher altitudes. An example of such a butterfly species is the small mountain ringlet, Erebia epiphroiz, a species which is usually to be found in mountainous areas of England and Scotland well above 400m. It is likely that such cold-adapted species will move to higher altitudes as average temperatures increase, but eventually there may be nowhere for them to go and they will become extinct.

Observed effects Evidence of the impact of climate change on UK insect pests

Potential effects of climate change on insects

must be tested against real data. There has already been some evidence of a 0.5degC rise in temperature this century and a significant positive trend in the temperature in the North- ern Hemisphere since 1964 (Jones and Wigley 1990). Have these changes already led to significant changes in insect populations?

To answer such questions requires long runs of carefully collected quantitative data. Unfor- tunately, such data are relatively rare. Distribu- tion data have been collected at irregular intervals since the 1960s through the various schemes co-ordinated by the Biological Re- cords Centre of the Institute of Terrestrial Ecology (ITE), but continuous runs of quantitative data on terrestrial invertebrates are only available on aphids and moths from the suction- and light-trap networks of the Ro- thamsted Insect Survey (Taylor 1986; Woiwod and Harrington 1994) and ITES butterfly- monitoring scheme (Pollard and Yates 1993).

Analysis of these databases for convincing evidence of climate change effects on insect populations is only just beginning but there is already a suggestion that the phenologies offive aphid species so far examined have changed consistently with climate change predictions (Fleming and Tatchell 1994). Similar changes are to be found in the Insect Surveys moth data (R. A. Fleming, personal communication).

Evidence from unusual weather events

Another approach to testing theoretical predictions is to look at the effects that have been observed in years, or runs of years, with un- usually mild winters and high spring and summer temperatures. Fortunately, a recent series of such years exists (1988-90) and because of current interest in global warming a concerted effort was made to collect all relevant observations together for the UK (Cannell and Pitcairn 1993). From autumn 1988 to autumn 1990 average temperatures were above normal in most of the UK, rainfall was low in the south- east, and there were two successive mild winters and hot summers with an extended drou- ght in east and central England.

Observations were largely as predicted:

(i) Populations of species with active winter

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stages such as aphids increased particularly in 1989, but there was some evidence that aphid predators such as ladybirds and hoverflies built up and prevented pest outbreaks in 1990.

(ii) Some migrant species were able to overwinter successfully.

(iii) Spring flying aphids, moths and butterflies appeared earlier than usual and as predicted, despite extrapolation beyond the limits of previous data.

(iv) Aphid-borne virus diseases were a severe problem in 1990.

(v) Cutworms and carrot fly also caused problems for vegetable growers.

One interesting species omitted from the report was the carabid beetle, Zubrus ten- ebrioides. This is an established pest of cereals in continental Europe and, although resident, is a relatively rare species in Britain. The first reported pest outbreak of this species was in a field in Cambridgeshire in 1977 following the hot summer of 1976 (Bassett 1978). This species was reported again as a pest in cereal fields after the hot summers of 1989 and 1990 on the South Downs and near Slough. This is clearly a resident species that requires hot summers and mild winters to build up populations to outbreak levels. Recently, a joint research project between British and Bulgarian entomologists has been set up to study the biological control of this species. This is a good example of the type of species which may cause UK agriculture considerable problems in a future warmer climate.

At the time of writing, we are coming to the end of the mildest November on record. It is far too early to say what the winter will herald for next year in terms of pests but, from the entomologists viewpoint, if not the farmers, it is off to an interesting start.

Acknowledgements

The aphid work described is funded by the Biotechnology and Biological Sciences Re- search Council, the Ministry of Agriculture, Fisheries and Food, the Natural Environment Research Council, the Home Grown Cereals Authority and Sugar Beet Research and Educa-

tion Fund. We are grateful to all of these. We greatly appreciate the efforts of all trap oper- ators and the Rothamsted Insect Survey and Scottish Agricultural Science Agency staff over many years.

References Bassett, P. (1978) Damage to winter cereals by Zabrus

tenebriozifes (Goeze) (Coleoptera: Carabidae). Plant Pathol., 27, p. 48

Cammell, M. E. and Knight, J. D. (1992) Effects of climatic change on the population dynamics of crop pests. Adv. Ecol. Res., 22, pp. 117-161

Cannell, M. G. R. and Pitcaim, C. E. R. (Eds.) (1993) Impacts ofthe mild w i n m and hot summers in the United Kingdom in 1988-1990. Department of the Environ- ment, HMSO, London

Carter, D. J. (1984) Pest LEpzdoptera of Europe - with special refmeme to the British Isles. Junk, Dordrecht, 431 pp.

Collier, R. H., Finch, S., Phelps, K. and Thompson, A. R (1991) Possible impact of global warming on cabbage root fly (Delia radicum) activity in the UK. Annals. Appl. Biol., 118, pp. 261-271

Dennis, R. L. H. (1993) Butterjlks and climate change. Manchester University Press, Manchester, 302 pp.

Department of the Environment (1991) The potential effects of climate change in the United Kingdom. United Kingdom Climate Change Impacts Review Group, First Report, HMSO, London

Dewar, R. C. and Watt, A. D. (1992) Predicted changes in the synchrony of larval emergence and budburst under climatic warming. Oecologia, 89, pp. 557-559

Fleming, R. A. and Tatchell, G. M. (1994) Long term trends in aphid flight phenology consistent with global warming methods and some preliminary re- sults. In: Leather, S. R., Watt, A. D., Mills, N. J. and Walters, K. F. A. (Eds.) Indzzduals, populations and panems in ecology. Intercept, Andover, pp. 63-71

Harrington, R., Tatchell, G. M. and Bale, J. S. (1990) Weather, life cycle strategy and spring populations of aphids. Acta Phytopathol. Enwmol. Hung., 25, pp. 423432

Harrington, R., Hulle, M., Pickup, J. and Bale, J. (1992) Forecasting the need for early season aphid control: geographical variation in the relationship between winter temperature and early season fight activity of Myzus persicae. In: Moniwnng and fmecast- ing w improve m p and environmentproteceion, Associa- tion of Applied Biologists, Warwick, pp. &11

Harrington, R. and Stork, N. E. (Eds.) (1995) Insects in a changing enzironment. 17th Symposium of the Royal Entomological Society, Academic Press, London,

Jones, P. D. and Wigley, T. M. L. (1990) Global

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warming trends. Sci. Am., 263, pp. 66-73

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The greenhouse effect and the future of UK agncul- ture. J. R. Agnc. Soc., 150, pp. 120-121

Pollard, E. and Yates, T. J. (1993) Monztonng butterjflies for ecobgy and conservation. Chapman Hall, London, 274 pp.

Porter, J. H. (1995) The effects of climate change on the agncultural environment for crop insect pests with particular reference to the European corn borer and grain maize. In: Harrington, R. and Stork, N. E. (Eds.) Insects in a chungzng environment, 17th Sym- posium of the Royal Entomological Society, Aca- demic Press, London, pp. 93-123

Porter, J. H., Parry, M. L. and Carter, T. R. (1991) The potential effects of climatic change on agncultural insect pests. Agric. For. Meteorol., 57, pp. 221-240

Sutherst, R. W., Maywald, G. F. and Skarratt, D. B. (1995) Predicting insect distributions in a changed climate. In: Harrington, R. and Stork, N. E. (Eds.) Insects in a changing envzronwenr, 17th Symposium of the Royal Entomological Society, Academic Press, London, pp. 59-91

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pp. 195-205

Football 1: Weather 1

Greg Spellman Nene College, Northampton

In order to lend support to those who advocate that sport is a metaphor for life one could point to the last four World Cup football tournaments and compare them to the general concern about global warming. Reports in the media of these events were sometimes dominated by anxiety about the heat and humidity suffered by players rather than the games themselves. In fact at the recent tournament in the USA one commentator writing in the Guardian went as far as saying that the weather over most of the country has been so extreme that the games have been tests of survival not skill (Guardian, 22 June 1994). Even a committed football enemy would have been hard-pressed not to hear about these energy- sapping weather conditions in the USA. After all, the Republic of Ireland, according to their manager Jackie Charlton, were not actually beaten by a more skilful higher-scoring Mexico team but by the weather.

This also seems to have been the case in the recent finals in Italy 1990 (with temperatures

exceeding 37C in a July heatwave) and Mex- ico 1986. In addition, Spain 1982 had many amateur biometeorologists consulting their ther- mal discomfort charts and busily calculating their own personal versions of the temperature-humidity index. Ron Greenwood (the then England manager) estimated that the temperature on the pitch in Bilbao (England versus France) was as high as 110F (43C; all football temperatures are recorded in Fahrenheit - it sounds hotter!) and considered that heatstroke could have become a real danger. He also revealed that most players during the 90 minutes had shed 3kg and Paul Mariner (Ipswich Town stalwart) had lost 5 kg - a remarkable 55 g per minute - forcing him to drink 5 litres of liquid after the game (The Times, 18 July 1982).

In the USA the problems of midsummer temperatures were exacerbated by the need to start many games at noon and that meant players were playing at the hottest part of the day. The organ- isers, FIFA, did say that it was not pandering to TV producers but trymg to avoid a global workforce falling asleep having stayed up half the previous night watching football. What was even more bizarre was the fact that some of the games were held indoors. Before the tournament it was

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Insect crop pests and the changing climate