Rapid cold hardening capacity in five species of coleopteran pests of stored grain

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Abstract

The capacity for rapid cold hardening was examined in recently-eclosed adults of five coleopteran species associated with stored grain. Supercooling points indicated that mortality was predominantly due to chilling injury. Threshold temperatures for indirect chilling injury for each of these species were determined by fitting survivorship data for unacclimated insects held for 0–6 h at various sub-0°C temperatures to a response surface. These response surfaces were used to predict a threshold temperature for each species at which 50% of the unacclimated individuals would survive for 2 h. The survival time at this threshold temperature with acclimation for 2 h at 4°C was compared to that without acclimation. The ratio of the 50% survivorship time of unacclimated to that of acclimated beetles was 8.7 for C. ferrugineus. This exceeded by over two-fold the range of 2.6–4.0 observed for the remaining species indicating that, in addition to greater innate cold hardiness, C. ferrugineus also has a greater capacity for rapid cold hardening than the other species examined.

Introduction

Cold tolerance of insects at sub-0°C can be increased by short exposures (e.g., 2 h) to temperatures of 0–5°C. This phenomenon has been called “rapid cold hardening” (Lee et al., 1987) to distinguish it from the seasonal acclimation or acclimatization processes in insects, which typically occur over periods of weeks (Lee, 1991). Rapid cold hardening was originally demonstrated in four species from the orders Coleoptera, Diptera, and Hemiptera (Lee et al., 1987), and has subsequently been demonstrated in several other insect species (e.g., Chen et al., 1990; Coulson and Bale, 1990; Czajka and Lee, 1990; Larsen et al., 1993; Rosales et al., 1993; Larsen and Lee, 1994). Interspecific comparisons have been made among dipteran species within the family Sarcophagidae (Chen et al., 1990) and of the genus Musca (Rosales et al., 1993), and within the homopteran genus Dalbulus (Larsen et al., 1993). But quantitative comparative measurements, such as the exposure time predicted to result in 50% survivorship for a given temperature (LT50), were not provided for the dipteran data. Interspecific comparisons among the homopteran data demonstrated seasonal differences in cold tolerance rather than rapid cold hardening. Because questions have been raised concerning the ecological and evolutionary significance of the rapid cold hardening phenomenon (Coulson and Bale, 1990, Coulson and Bale, 1991), more interspecific comparisons are warranted.

Increased tolerance of sub-0°C cold in these studies was not a result of changes in the supercooling point; thus, rapid cold hardening affected susceptibility to chilling injury rather than internal freezing. Chilling injury, i.e., cold injury in the absence of internal ice formation, can be direct or indirect (Morris and Watson, 1984; Lee, 1991). Direct chilling injury refers to acute injury and is thought to be due to damage to cell membranes (Morris and Watson, 1984), whereas indirect chilling injury refers to delayed mortality and is thought to be due to irreversible damage to cellular respiration (Morris and Watson, 1984; Hochachka and Dunn, 1986). In many single-celled organisms and single cells or cell lines from multi-cellular organisms, the temperature at which death from cold injury occurs with exposures of ≤2 h is a good predictor of whether injury is direct or indirect (Morris and Watson, 1984). Thus, this threshold for indirect chilling injury (ThresholdICI) offers a way to compare cold injuries which produce a similar impact between species differing in innate (i.e., unacclimated) cold tolerance.

Insect pests of stored grain are a logical model system with which to examine the ecological significance of the rapid cold hardening process. Because many of these species are easily reared in the laboratory and the cold hardiness of these pests is economically important, there is a large amount of literature on cold hardiness in stored product insect pests (Howe, 1965; Evans, 1983; Fields, 1992). Some of these species can also be viewed as an ecological guild. For example, the species we examined—Cryptolestes ferrugineus (Stephens) and Oryzaephilus surinamensis (L.), (Cucujidae); Rhyzopertha dominica (F.) (Bostrichidae), Sitophilus oryzae (L.) (Curculiondiae); and Tribolium casteneum (Herbst) (Tenebrionidae)—are all commonly found in wheat stored in the US Plains states. All stages may overwinter, and no overwintering diapause has been found in these species. Young adults of R. dominica are more tolerant of prolonged cold temperature than larvae (Hagstrum and Flinn, 1994), and the adult is the most cold-tolerant stage of C. ferrugineus (Smith, 1970). We wished to compare the magnitude and assess the variation of rapid cold hardening capacity in these five species that, in their usual habitat, are sheltered from both low sub-0°C temperatures and large, rapid, temperature fluctuations. In this habitat, there would seem to be little selection favoring rapid cold hardening and one would predict a uniformly low capacity for rapid cold hardening compared to species subjected to greater environmental fluctuations.

In this study, we compare the magnitude of the rapid cold hardening response in young adults of five species. To distinguish between chilling and freezing injury, we examined supercooling points. In order to estimate the ThresholdICI, we first used a previously described model (Hagstrum and Flinn, 1994) to help find the temperature for which a 2-h exposure resulted in 50% survival. The effect of rapid cold hardening (acclimation for 2 h at 4°C) was compared among these species. In order to make quantitative comparisons of the rapid cold hardening effect, we examined the ratio between the LT50 values for acclimated vs. unacclimated beetles.

Section snippets

Insects

The R. dominica colony used in this study was established from adults collected in Dickinson County, Kansas within a year of the study. Other species were from laboratory colonies which had long been maintained in the Grain Marketing and Production Research Center in Manhattan, Kansas. Tribolium castaneum were reared on flour with 5% (weight:weight) brewer’s yeast added (Tribolium diet). Oryzaephilus surinamensis were reared on a diet of two parts rolled oats and one part Tribolium diet

Results

Median crystallization temperatures varied between species (Fig. 1), but 2-way ANOVA revealed no statistically significant effects of acclimation on supercooling points. The highest supercooling points were found among R. dominica, in which 19% of the individuals tested (12/58) froze internally at temperatures higher than −12°C. Among the other species examined, the 90th percentile supercooling point was less than the temperature at which cold survivorship was examined (≥−14° for C. ferrugineus

Discussion

This study differs from previous examinations of rapid cold hardening in using the temperatures with the same physiological impact for each species to compare their capacity for rapid cold hardening, rather than the same temperature. In the current and previous studies (Howe, 1965; Fields, 1992), C. ferrugineus was more cold hardy than the other species. Our findings indicate that C. ferrugineus also has a greater capacity for rapid cold hardening in young adults than other species.

Rapid cold

Acknowledgements

We acknowledge the assistance of B. Bachellor, S. Nicholls, and Z. Tavakkol in rearing the insects used in these studies. B. Barnett assisted with the crystallization temperature determinations.

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