TY - JOUR
AU1 - Sitz, Rachael, A
AU2 - Peirce, Erika, S
AU3 - Luna, Emily, K
AU4 - Cockrell, Darren, M
AU5 - Newhard, , Laura
AU6 - Peairs, Frank, B
AB - Abstract Brown wheat mites, Petrobia latens (Müller 1776, Acari: Tetranychidae), are sporadic yet economically damaging pests of winter cereals. In Colorado, their life history is closely tied to the development of winter wheat, where they are present in the field from crop planting in late September through harvest in early June. In order to withstand winter months, these mites are able to survive cold temperatures. However, the mechanisms of cold hardening and their temperature limits are unknown. This research documents the seasonal supercooling points of the brown wheat mite. Their seasonal average supercooling point stayed consistent throughout the year, never varying more than a degree from the overall average supercooling point of −17°C. The greatest variation in supercooling point was seen in the spring, during which supercooling point temperatures ranged from −9.2 to −25.5°C. We also documented the upper and lower lethal temperatures for the brown wheat mite. When comparing small nymphs to large nymph and adult stages, small nymphs were slightly more cold tolerant (lethal temperature estimates required to kill 99% of the population [LT99] were −30.8 and −30.6°C, respectively), but less heat tolerant (LT99 was 50 and 56°C, respectively). lethal temperatures, supercooling point, cold tolerance Brown wheat mites, Petrobia latens, Müller, 1776 (hereafter referred to as BWM), are highly mobile spider mites (Acari: Tetranychidae) that feed on a wide range of hosts, including several winter cereals (Cox and Lieberman 1960). BWM sucking damage reduces plant growth (Khan et al. 1969) and in high infestations can cause economic losses. In the United States, BWM outbreaks are historically sporadic and almost exclusively recorded following dry weather events (Fenton 1951, Broadley 1982). BWM was first described in California and New Mexico in the early-1900s (Banks 1912), but in the mid-1900s, it was documented broadly throughout the Western United States (Ewing 1921, Fenton and Whitehead 1944, Knowlton and Tibbetts 1952). More recently, outbreaks have been reported during drought conditions in the central United States High Plains wheat growing regions (Depew 1968, Blodgett et al. 2002, Maxmen 2013;Peairs et al. 2014, Bradshaw, pers. website). Damage often results in yellowing or bronzing of the leaves and begins at the tip of the leaf (Singh 1985). BWM do not produce webbing and they frequently travel from plant vegetation into protected crevices in the ground when stimulated by less than optimal weather conditions or movement (Khan et al. 1978). Therefore, in some cases plant damage is the only indication of an infestation. Weather conditions, such as heavy rainfall, can destroy most of the BWM populations (Cox 1960). There is evidence that BWM requires both dry and moist conditions to complete development (Cox 1960). However, not much is known on how temperature affects BWM mortality. The ability to withstand extreme temperatures is a crucial factor in the geographical distribution of an arthropod species and imperative for survival and success in various regions (Graham 1924). Injury from temperature extremes can be acute immediate damage to cells, chronic slow damage to cells, or latent where fitness is reduced later in life (Sinclair and Roberts 2005). The onset of decreasing temperature is the cue to begin physiological changes, and the cold-hardiness of arthropods gradually increases as the temperature changes (Lee et al. 1987). Arthropods able to survive in cold temperatures are broken up into two categories including freeze tolerant and freeze intolerant. The supercooling point is reached upon ice nucleation in an arthropod. Freeze tolerant species can withstand formation of ice crystals within their bodies, in contrast to freeze intolerant species, which are killed (Salt 1961, Denlinger and Lee 2010). The objective of this study was to better understand the thermal extremes of BWM and to predict overwintering conditions. Methods Brown Wheat Mite Sampling BWM samples were taken with a Vortis suction sampler made from a modified Husqvarna 125BV blower (Husqvarna Group, Stockholm, Sweden). Mites were obtained from wheat fields and adjacent buffer strips consisting of alternating blocks of crested wheat grass (Agropyron cristatum L.) and intermediate wheat grass (Thinopyrum intermedium [Host] Barkworth and Dewey), which historically experienced consistent BWM infestations. Fields were in a wheat-fallow rotation and located at Colorado State University’s Agricultural Research and Development and Education Center, Fort Collins, CO (GPS: 40.6542, −104.9979). Samples were transferred to the Insectary Laboratory at Colorado State University, where BWM were separated from the samples and stored at 4°C until used in the experiments. Supercooling Point Determination BWM samples were obtained monthly for supercooling point (SCP) determination. Supplies and methods were similar to Luna et al. (2013), where mites were adhered between a 36-guage copper wire thermocouple and an aluminum rod with a paintbrush and high vacuum grease (Dow Corning, Midland, MI). The apparatus fit into an aluminum block inside of an environmental test chamber programmable freezer (Tenny Jr. Programmable Freezer, Tenny, Inc., South Brunswick, NJ). The initial chamber temperature was set at 0°C and decreased at a rate of 0.2°C/min until it reached −30°C. A data logger recorded the temperatures every second (DaqPro-5300, Portable Handheld Data Logger, Omega Engineering, Inc., Stamford, CT), and the accompanying software was used to generate graphs of the data. A temperature increase signified the release of heat from the mite upon supercooling. About 12–24 h after the experiment, mortality was confirmed when mites were disturbed with a paintbrush and did not initiate movements. Lower and Upper Lethal Temperature Determination In total, 1,188 live BWM were used in the four lethal temperature experiments. Individual BWM were sorted by respective size class: either large nymphs and adults (n = 202), or small nymphs (n = 986) (Khan et al. 1969). There were eight temperature treatments in each of the four experiments; therefore, large and small mites were divided into 32 groups. Groups of mites were placed in 1-ml plastic microcentrifuge tubes, and then in a paper bag labeled with the temperature treatment. In the two lower lethal temperature (LLT) experiments, the temperature in the programmable environmental test chamber was held at 25°C for 12 h then decreased at a rate of 4°C/h until reaching −23°C. Specimens were removed at each of the following predetermined temperatures: 0, −5, −10, −13, −15, −18, −20, and −23°C. Mites were then checked for survival after 30 min at 4°C, and the number of eggs deposited by each group of mites was recorded. In the two upper lethal temperature (ULT) experiments, BWM were placed into the programmable environmental test chamber and held at 26°C for 7 h. The temperature in the chamber was then increased at a rate of 4°C/h to 60°C. Mites were removed from the chamber at the following temperatures: 28, 34, 40, 46, 50, 54, 57, and 60°C. To account for a gain in function after heat exposure, mites were held at room temperature for 22–28 h before survival data were recorded. The number of eggs deposited by BWM in the ULT experiments was also recorded. After the lethal temperature experiments, specimens were deposited in the C. P. Gillette Museum of Arthropod Diversity at Colorado State University. Statistical Analysis The SCP experiment ran from January through December 2014. Months were grouped into seasons. To account for non-normality in the seasonal SCP data, the Dunn’s test with Control for Joint Ranks was used to detect differences in mean temperatures (JMP Statistical Software, 11.1.0v; SAS Institute, Cary, NC). For the ULT and LLT experiments, data consisted of the number of live or dead individuals and were used to calculate percent mortality at each temperature. Logistic regression was used to calculate lethal temperatures for 50 and 99% mortality (LT50 and LT99, respectively) at upper and lower temperature extremes for large and small nymphs (PROC LOGISTIC, SAS Institute Inc. 2014). Due to background mortality in the upper lethal temperature determination study, an offset constant was required for logistic regression equations (C = 0.4873 large nymphs per adult and C = 0.6196 for small nymphs). A t-test was used to compare the number of eggs laid by mites in the upper and lower lethal temperature experiments. A linear model analysis of variance was performed, and then a Tukey’s honestly significantly different test analyzed differences among temperature treatments (JMP Statistical Software, 11.1.0v; SAS Institute). Graph visualizations were conducted using R 3.5.0 and ggplot2 3.1.1. (Wickham 2016). Results Supercooling Point Mite stage in the field varied considerably through time. Mites were observed on grasses between September and April. Monthly mite SCP were tested in January, February, March, April, May, June, October, and December, and grouped together into seasons (winter: February, December, January; spring: April, May; summer: June; and fall: October). SCP temperature ranged from −9.2 to −25.5°C, with both extremes occurring during the spring. Mean SCPs were −17.9, −17.3, −16.4, and −16.7°C for spring, summer, fall, and winter, respectively (Fig. 1). Seasonal comparisons showed no differences existed between any of the seasons (P > 0.05), but winter and summer supercooling temperatures contrasted each other more than all other seasonal comparisons (P = 0.0542). There was 100% mortality once mites reached their SCP. Fig. 1. Open in new tabDownload slide Seasonal supercooling points for the brown wheat mite, P. latens, are shown for spring (April 2014, May 2014; n = 23), summer (June 2014; n = 6), winter (February 2014, December 2014, January 2015; n = 53), and fall (October 2014; n = 18). Points are jittered to show distribution. Diamonds indicate averages. Fig. 1. Open in new tabDownload slide Seasonal supercooling points for the brown wheat mite, P. latens, are shown for spring (April 2014, May 2014; n = 23), summer (June 2014; n = 6), winter (February 2014, December 2014, January 2015; n = 53), and fall (October 2014; n = 18). Points are jittered to show distribution. Diamonds indicate averages. Lower and Upper Lethal Temperature Determination BWM mortality at −20°C was 85% for large mites, 78% for small mites, and at −23°C mortality was 100% for both groups (Fig. 2A). Lower median lethal temperatures (LT50) were −12.8 and −15.9°C for large and small mites, respectively, and lower lethal temperature estimates required to kill 99% of the population (LT99) were −30.6 and −30.8°C, respectively (Table 1). The logistic regression for lower lethal temperatures for large mites (R2 = 0.74, n = 106) is y = exp(−3.30 + −0.26x)/(1 + exp(−3.30 + −0.26x)), where y is the probability of mortality and x is temperature, and for small mites (R2 = 0.84, n = 412) is y = exp(−4.90 + −0.31x)/(1 + exp(−4.90 + −0.31x). Table 1. ULT and LLT estimates required to kill 99% (LT99) or 50% (LT50) of the population for the brown wheat mite, P. latens Petrobia latens size class Upper LT50 (°C) Upper LT99 (°C) Lower LT50 (°C) Lower LT99 (°C) Large 48.0 56.0 −12.8 −30.6 Small N/A 55.0 −15.9 −30.8 Petrobia latens size class Upper LT50 (°C) Upper LT99 (°C) Lower LT50 (°C) Lower LT99 (°C) Large 48.0 56.0 −12.8 −30.6 Small N/A 55.0 −15.9 −30.8 Lethal temperature estimates are derived from the logistic regressions.. Open in new tab Table 1. ULT and LLT estimates required to kill 99% (LT99) or 50% (LT50) of the population for the brown wheat mite, P. latens Petrobia latens size class Upper LT50 (°C) Upper LT99 (°C) Lower LT50 (°C) Lower LT99 (°C) Large 48.0 56.0 −12.8 −30.6 Small N/A 55.0 −15.9 −30.8 Petrobia latens size class Upper LT50 (°C) Upper LT99 (°C) Lower LT50 (°C) Lower LT99 (°C) Large 48.0 56.0 −12.8 −30.6 Small N/A 55.0 −15.9 −30.8 Lethal temperature estimates are derived from the logistic regressions.. Open in new tab Fig. 2. Open in new tabDownload slide (A) Lower lethal temperatures for brown wheat mite, P. latens, exposed to a gradient of low temperatures were determined by percent mortality for large (n = 106), and small (n = 412) mites. (B) Upper lethal temperature determination for large (n = 96), and small (n = 574) mites when exposed to increasing temperatures. Fig. 2. Open in new tabDownload slide (A) Lower lethal temperatures for brown wheat mite, P. latens, exposed to a gradient of low temperatures were determined by percent mortality for large (n = 106), and small (n = 412) mites. (B) Upper lethal temperature determination for large (n = 96), and small (n = 574) mites when exposed to increasing temperatures. For ULT, mortality for small mites was 97% at 54°C and 100% at 57°C, whereas for large mites’ mortality was 99% at 57°C, and 100% at 60°C (Fig. 2B). The LT50 for large mites was 48°C and was not calculated for small mites due to high background mortality. LT99 for large and small mites was 56 and 50°C, respectively. Further, an offset constant was required for the logistic regression equations documenting BWM mortality when exposed to increasing temperatures (C = 0. 4873 for large mites and C = 0.6196 for small mites). The regression equation for upper lethal temperatures for large mites (R2 = 0.51, n = 96) is y = 0.49 + ((1 − 0.49) × exp(−53.09 + 1.02x)/(1 + exp(−53.09 + 1.02x))) and small mites (R2 = 0.46, n = 574) is y = 0.62 + ((1 − 0. 62) × exp(−32.44 + 0.65x)/(1 + exp(−32.44 + 0.65x))). When comparing upper and lower temperature treatments, fewer eggs were observed in the lower temperature treatments (9 eggs vs 154 eggs [P < 0.0001]). However, no differences in egg number were detected among the eight upper or lower temperature treatments (P = 0.29 and P = 0.77, respectively). Eggs were only laid by BWM in the large nymph/adult group. Discussion Supercooling Point Peak mite activity in Colorado was similar to field studies done by Cox and Lieberman (1960) in Utah, although nymphs were more abundant in Colorado during September when compared to Utah. BWM have a consistent SCP as ambient temperature changes, indicating limited acclimation throughout the year. Conversely, two-spotted spider mites, another pest of crops in Colorado, have distinct nondiapausing and diapausing stages that have a varied SCP throughout the year (Khodayari et al. 2013a, b). Although these mites can withstand temperatures below freezing (indicating they are a cold tolerant species), they cannot withstand ice formation in their body water. Ice nucleation occurred at the SCP, and the mites did not survive. This demonstrates that they are freeze intolerant (Salt 1961, Denlinger and Lee 2010). The large variation in SCP temperatures in the spring is likely attributed to differences in the mite stage tested during this time of year. Here, LLT experiments found that smaller mites tended to be more cold-hardy, a phenomenon that is described in other invertebrate poikilotherms (Block 1982, Colinet et al. 2007). Therefore, younger mite stages collected in the spring may have a lower SCP than their adult counterparts. In addition to this, no differences existed between any of the seasons, suggesting that they are somewhat tolerant to unseasonably cold weather during warm seasons. Results from SCP and LLT experiments differed in the ultimate temperature, with LLT ~5°C lower. This discrepancy is likely due to differences in experimental design. In the SCP experiment, mites were directly exposed to cold temperatures, whereas when determining LLT, mites were placed in plastic tubes with conspecifics which may have acted as a buffer. Interestingly, winter temperatures regularly fall below the average SCP, suggesting that BWM inhabit microclimates to buffer cold temperatures. BWM are highly mobile, and likely seek the protection of leaf litter and plant debris. Furthermore, snow can insulate insects in below-ground overwintering locations (Khan et al. 1969) and could provide protection to BWM. Cooling rate for the SCP experiment was faster than for the LLT experiment, which may also be a factor for the difference. LLT and ULT Determination Based on the logistic regression equations, LLT estimated to kill mite populations were consistently lower for small mites when compared with large mites, suggesting that nymphs are more cold tolerant than adults. In contrast, adult mites were able to survive temperatures around 3°C higher than nymphs. While there were less eggs laid during the LLT experiment, there were no differences in the type of egg that was laid. All eggs laid were considered red nondiapause eggs as they were consistent with Lees (1961) description. In conclusion, BWM are a freeze-intolerant species that likely employ a variety of behavioral and physiological adaptations to avoid ice nucleation in their bodies while overwintering in temperate climates. In addition, BWM nymphs can survive colder temperatures than adults and egg laying occurs more frequently during heat stress. Further work is required to evaluate why this pest is periodically a problem and what information is needed to predict outbreaks. Future research should investigate the interactions between temperature and relative humidity on fecundity as well as evaluate how land complexity and changing microclimates influence survivability of BWM. Importantly, these experiments demonstrate that the SCP of BWM is higher than the lowest air temperatures experienced during Colorado winters, which suggests that microclimates play an important role in the survival of this pest. Acknowledgments We thank members of the CSU Insectary. 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This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - Temperature Limits for the Brown Wheat Mite, in Colorado
JF - Journal of Economic Entomology
DO - 10.1093/jee/toz157
DA - 2019-09-23
UR - https://www.deepdyve.com/lp/oxford-university-press/temperature-limits-for-the-brown-wheat-mite-in-colorado-w59Vi0Pf7o
SP - 2507
VL - 112
IS - 5
DP - DeepDyve
ER -