Population Dynamics of Aphids on Cereals: Digging in the Time-Series Data to Reveal Population Regulation Caused by Temperature

Martinkova Z (2014) Population Dynamics of Aphids on Cereals: Digging in the Time-Series Data to Reveal Population Regulation Caused by Temperature. PLoS ONE 9(9): e106228. doi:10.1371/journal.pone.0106228 Population Dynamics of Aphids on Cereals: Digging in the Time-Series Data to Reveal Population Regulation Caused by Temperature Marek Brabec 0 Alois Hone k 0 Stano Peka r 0 Zdenka Martinkova 0 Thomas L. Wilkinson, University College Dublin, Ireland 0 1 Department of Nonlinear Modeling, Institute of Computer Science of the Academy of Sciences of the Czech Republic , Prague, Bohemia , Czech Republic , 2 Department of Invertebrate and Plant Biodiversity in Agrosystems, Crop Research Institute , Prague, Bohemia , Czech Republic , 3 Department of Botany and Zoology, Faculty of Science of the Masaryk University , Brno, Moravia , Czech Republic Aphid populations show periodic fluctuations and many causes are attributed to their dynamic. We investigated the regulation by temperature of the aphid populations composed of Metopolophium dirhodum, Sitobion avenae, and Rhopalosiphum padi on winter wheat using a 24 years long time series data. We computed the sum of daily temperatures above 5uC, the threshold temperature for aphid development, and the sum of daily temperatures within the [0(threshold for wheat development),5] uC interval. Applying Generalised Additive Model framework we tested influences of temperature history expressed via degree days before the start of the aphid immigration on the length of their occurrence. We aimed to estimate the magnitude and direction of this influence, and how far to the past before the start of the aphid season the temperature effect goes and then identify processes responsible for the effect. We fitted four models that differed in the way of correcting for abundance in the previous year and in specification of temperature effects. Abundance in the previous year did not affect the length of period of aphid population growth on wheat. The temperature effect on the period length increased up to 123 days before the start of the current season, i.e. when wheat completed vernalization. Increased sum of daily temperatures above 5uC and the sum of daily temperatures within the [0,5] uC interval both shortened the length of period of aphid population growth. Stronger effect of the latter suggests that wheat can escape from aphid attacks if during winter temperatures range from 0 to 5uC. The temperature influence was not homogeneous in time. The strongest effect of past temperature was about 50 to 80 and 90 to 110 days before the beginning of the current aphid season indicating important role of termination of aphid egg dormancy and egg hatching. - Funding: This work received support from these sources: Long-term strategic development financing of the Institute of the Computer Science project no. RVO 67985807 (MB); Ministry of Agriculture of the Czech Republic project no. RO 0414 (AH and ZM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Population size of organisms fluctuates in time and space due to variety of reasons, such as fluctuations in environmental conditions, availability of resources and impact of enemies. Changes in population numbers are variable but some general patterns have been revealed: large fluctuations occur in animals that occupy larger areas [1], have higher reproductive potential [2], are of smaller size [3] or are trophically specialized [4]. Aphids are economically significant pests attacking variety of crops. A considerable annual variation in aphid population numbers has been frequently observed. For example, in a previous study on winter wheat aphids in the central Czech Republic [5], the peak abundance varied during an 18-year period by two orders of magnitude. The aphids on cereals form a multispecies complex [68]. Such parallel occurrence of several aphid species is determined by similar life history: the species are holocyclic though overwintering on different primary hosts [9]. Dominant species are Metopolophium dirhodum (Walker) and Rhopalosiphum padi (L.), both heteroecic with eggs overwintering on roses (Rosa spp.) and bird-cherry (Prunus padus L.) respectively, and Sitobion avenae (F.), monoecic with eggs overwintering on grasses. The seasonal fluctuation in their dynamic is determined by population growth rate and length of the period for which the population can grow. After passing few generations on the primary host in the spring, migration to cereal stands occurs in mid May at the cereal development stage of stem extension (Zadoks scale 31 32). Parthenogenetic females have high reproductive potential due to short generation time caused by telescopic mode of reproduction [10], which results in quick succession of generations and a high intrinsic rate of population increase. Aphid abundances grow quickly and may attain more than 100 individuals per tiller in late June or early July [11]. The peak is followed by an abrupt decline caused by host plant senescence and spreading of mycoses [12]. Aphid abundance plotted over time has thus a left-skewed triangular shape. The growth rate of aphid populations is affected by host plant quality (species and cultivars) and environmental conditions, particularly soil fertility and crop stand density resulting in intraspecific competition. Predators and parasitoids limit population growth as the population peak approaches [13]. Different factors were advocated in search for explaining cyclic dynamic of aphids: long-term trends in agriculture practices [5], weather changes [14], natural enemy abundance, and intraspecific competition [15]. Establishing causes of annual changes in aphid populations is of high interest and practical importance to farmers. Here we focused on a hypothesis that annual variation of aphid populations is driven by temperature. Their maximum abundance is determined largely by duration of the period of aphid population growth. The onset of this period in the spring is determined by aphid migration to cereal stands, and the end of the period in summer is terminated by host plant maturation. Both processes are temperature driven but determined by different thermal constants. Lower thermal threshold for aphids was established by a number of authors who indicated the lower threshold to be between 06uC [1620]. It is higher than that of the winter wheat which is virtually 0uC at early stage of development [21]. At later developmental stages the threshold for wheat may be higher and vary between cultivars [22]. Winter and early spring temperatures thus determine stage when aphids arrive on wheat crop and the length of period available to them before the onset of plant senescence. Winter temperatures between 05uC allow wheat development, postpone development of crop at which aphids arri (...truncated)