TY - JOUR
AU - Zhao, Fei
AB - Abstract Diurnal temperature fluctuations in nature can have a significant effect on many ectodermic traits. However, studies on the effects of diurnal temperature fluctuations on organisms, especially the effects on specific life stages, are still limited. We examined the immediate effects of the same average temperature (25°C) and different temperature amplitudes (±4, ±6, ±8, ±10, ±12°C) on the development and survival of Plutella xylostella (Lepidoptera: Plutellidae). We also assessed carry-over effects on adult longevity, reproduction, development, and survival of offspring across generations. The effect of moderate temperature amplitudes was similar to that of constant temperature. Wide temperature amplitudes inhibited the development of pupae, reduced total reproduction, lowered intrinsic rates of population growth, and slowed the development and survival of eggs on the first day, but the proportion of females ovipositing on the first three days increased. Insects coped with the adverse effects of wide temperature amplitudes by laying eggs as soon as possible. Our results confirmed that a logistic model based on daily average temperature cannot predict development rates under wide temperature amplitudes. These findings highlight the effect of environmental temperature fluctuations at the pupal stage on the development and oviposition patterns of P. xylostella and should be fully considered when predicting field occurrence. thermal amplitude, carry-over effect, transgenerational effect, pupal stage, Plutella xylostella Temperature is one of the most important environmental factors, affecting all aspects of life on earth (Gillooly et al. 2001, 2002; Buckley et al. 2016; Noble et al. 2018). The average temperature varies among different seasons, latitudes, and elevations, and there are daily temperature fluctuations between day and night in the natural environment. With global warming, the amplitude of temperature fluctuations has increased significantly as the average temperature has increased (Verheyen et al. 2019). Temperature fluctuations have a significant influence on many organisms (Paaijmans et al. 2013, Convey et al. 2015, Bozinovic et al. 2016), including fish (Joy et al. 2017), turtles (Sandmeier et al. 2016), lizards (Hulbert et al. 2017), and snakes (Patterson and Blouin-Demers 2008). For small ectotherms, the effects of temperature fluctuations may be even more pronounced. Temperature fluctuations have been shown to extend the development of Lucilia cuprina (Diptera: Calliphoridae) (Dallwitz 1984), shorten the developmental period of Sarcophaga argyrostoma (Diptera: Calliphoridae) and Lucilia illustris (Diptera, Calliphoridae) (Niederegger et al. 2010), improve the survival rate of Myzus persicae (Homoptera: Aphididae) (Davis et al. 2006), increase reproduction in Ceratitis capitata (Diptera: Tephritidae) (Terblanche et al. 2010), advance the eclosion time of Sarcophaga crassipalpis (Diptera: Sarcophagidae) (Miyazaki et al. 2011), improve the heat resistance of Drosophila melanogaster (Diptera: Drosophilidae) (Sørensen et al. 2005), and promote the synthesis of insect fatty acids, heat shock proteins, and amino acids (Bozinovic and Pörtner 2015, Colinet et al. 2018). However, wide temperature fluctuations also reduce the development rate of Plutella xylostella (Lepidoptera: Plutellidae) (Xing et al. 2014), reduce the survival rate of Sitobion avenae (Homoptera: Aphididae) (Zhao et al. 2019) and Plutella xylostella (Lepidoptera: Plutellidae) (Xing et al. 2015a, 2015b), decrease the reproduction of Sitobion avenae (Homoptera: Aphididae) and Rhopalosiphum padipadi (Homoptera: Aphididae) (Cao et al., 2018), reduce the longevity of S. avenae (Ma et al. 2015), decreased the intrinsic rate of natural increase of Tetranychus urticae (Acari: Tetranychidae) (Gotoh et al. 2014), decrease the pupal weight of Colias eriphyle (Lepidoptera: Pieridae) (Higgins, et al. 2015), lower the toxicant transmitting capacity of Aedes aegypti albopictus (Diptera: Culicidae) (Lambrechts et al. 2011, Paaijmans et al. 2010), decrease the cold tolerance of Ceratitis capitata (Diptera: Tephritidae) (Terblanche et al. 2010), and reduce the fertility of Tribolium confusum (Coleoptera: Tenebrionidae) (Estay et al. 2011). Thus, temperature fluctuations have potentially critical effects on insect development, survival, reproduction, and other activities. Different developmental stages of insects have different responses to temperature (Kingsolver et al. 2011, Zhao et al. 2017). The pupal stage is an important developmental stage for holometabolous insects, which undergo a drastic dissociation of the larval tissues and development of adult tissues (Skopik et al. 1967, Stevens 2004). Studies have shown that environmental temperature during the pupal stage has a significant effect on development, survival, longevity, reproduction, and population parameters. However, studies on the pupal stage most frequently use constant temperatures (Yamamoto et al. 2011, Skovgård and Nachman 2016), or short-term heat/cold shock treatments (Feder et al. 1997, Mahroof et al. 2005, Wang et al. 2016). Such experiments do not reflect the diurnal temperature fluctuations of the natural environment and ignore the repairing effects of cooler temperatures at night after high temperatures during the day. Other studies have used alternating temperatures (Yasuda et al. 1994, Scriber et al. 2011, Bear and Monteiro 2013, Falibene et al. 2016). In these experiments, insects are quickly transferred directly from one temperature to another, which is not consistent with the slow process of temperature change in nature, and also ignores the potential influence of the rate of temperature change on the life-history traits and heat resistance of insects (Mitchell and Hoffmann 2010). In some studies, the development and eye color of pupae (Peterson and Nilssen 1996, Resilva and Pereira 2014) and pupal survival rate (Peterson and Nilssen 1996) changed in insects following exposure to natural field temperatures; however, it is impossible to distinguish the influence of the average temperature from that of temperature fluctuations in the field. A few studies have examined the different effects of constant temperature and temperature fluctuations on pupal development, survival, growth, and weight ((Simmons 1993, Banahene et al. 2018) but, in general, these studies used average temperature change (Banahene et al. 2018) or only one amplitude of temperature fluctuation (Simmons 1993). In addition, most studies considered only the immediate effect of temperature on pupae (Peterson and Nilssen 1996, Fatemeh et al. 2018), or the carry-over effects on adult traits, for example, wing shape and size (Ottenheim and Volmer 1999), the size of the chest and abdomen (French et al. 1998), heat resistance and longevity (Zheng et al. 2017), reproduction (Zhang et al. 2015a), behavior (Telles-Romero et al. 2011), egg follicle maturation (Mohamed-Ahmed et al. 1994a, 1994b), or brain development (Falibene et al. 2016). The influence of temperature fluctuations during the pupal stage on key population parameters, or even delayed effects across generations, is unclear. The diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae), is an important pest worldwide, which mainly targets cruciferous vegetables (Chapman et al. 2010, Sarfraz et al. 2011). Temperature is one of the most important environmental factors that determine the occurrence of the diamondback moth. Previous studies have shown that temperature not only influences diamondback moth development (Golizadeh et al. 2007), survival (Guo and Qin 2010), and reproduction (Golizadeh et al. 2008), but also influences the migration path and regional distribution (Coulson et al., 2002). For example, the average temperature for June (approximately 25°C) does not differ notably between Wuhan (30.62 °N) and Beijing (39.80°N) in the main growing area of cruciferous vegetables in China but diamondback moths experience a significant difference in daily temperature amplitudes (Xing et al. 2019) (Supp Fig. 1 [online only]). Studies of the effects of temperature on the pupal stage of the diamondback moth have mainly assessed constant temperatures or alternating temperatures (Talekar and Shelton 1993, Marchioro and Foerster 2011, Xing et al. 2015). However, our previous studies have shown that temperature amplitude has a significant effect on the development and survival of eggs ((Xing et al. 2014, 2015b) and the development of the larval stages of the diamondback moth (Xing et al., 2019); the pupa, in the critical period of metamorphosis, may be even more sensitive to temperature change, which can have a significant effect on longevity, reproduction, and even population growth. Here, diamondback moth pupae were reared at six temperature amplitudes (±0, ±4, ±6, ±8, ±10 and ±12°C) with the same average temperature of 25°C. We studied the influence of temperature amplitudes on the development and survival of pupae, adult longevity and reproduction, as well as the development and survival of offspring. We aimed to determine 1) the immediate effect of temperature amplitude on pupae, 2) the carry-over effect of temperature amplitude on pupae and whether there are delayed effects across generations, 3) the effects of different temperature amplitudes experienced by pupae on population development. Materials and Methods Insects In May 2010, diamondback moth larvae were collected from a cabbage field in Wuhan (30.48°N 114.32°E), China. The larvae were raised on an artificial feed (Southland Products Inc., Lake Village, AR, USA) in the feeding room at 25 ± 1°C, 40–60% RH, and a light–dark cycle of 15:9 (L:D) h. Before the experiment, these larvae were kept in the feeding room for at least eight years. Experimental Protocol In this study, we used daily temperature data for the major cabbage-producing areas (Beijing, 39.80°N 116.47°E) in northern China in summer (June) (Xing et al. 2014). Preliminary analysis revealed that the average daily temperature was approximately 25°C in the summer, and the daily temperature amplitude was between ± 4 and ± 12°C. Therefore, in this study, the average simulated temperature was 25°C, and the temperature amplitudes were ±0, ±4, ±6, ±8, ±10, and ±12°C. Climate chambers (RXZ-380B-LED; Ningbo Jiangnan Instrument Factory, Ningbo, China) were used to set different temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C). The temperature cycle was set for 24 h and temperatures were set at hourly intervals with constant temperatures to simulate natural temperature fluctuations (Xing et al. 2019) (Supp Table 1 [online only]). Dataloggers (Hobo u23-001; Onset Computer Corporation, Bourne, MA, USA) were used to automatically record the actual temperature in different temperature amplitude chambers every 20 min (Xing et al. 2019) (Supp Table 2, Supp Fig. 2 [online only]). During the experiment, the photoperiod was set to 15 L: 9 D, in which the light stage was from 05:00 to 20:00 every day, and the dark stage was from 21:00 to 04:00. Humidity was controlled at 40–60% RH. Measurements Following ultraviolet light sterilization for 30 min, 1.7 ml of artificial feed was injected into each well to feed the larvae. Using a brush, newly laid eggs (the eggs laid by adults on the first day collected within 4 h of laying) were transferred to each well and placed in a holding room until the hatched larvae had pupated. Twenty-four-well perforated plates were covered with a fine nylon mesh (200 μm) to ensure adequate ventilation and then sterilized under ultraviolet light for 30 min. New pupae were placed individually into wells (within 4 h after pupation). In this experiment, we evaluated the effects of six temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C), with each amplitude treatment having three replicates, each comprising 24 new pupae. Thus, in total, we used 432 new pupae. All treatments were performed simultaneously. Pupal development and survival were monitored at 08:00 each day until pupal emergence or death. After eclosion, the newly eclosed females in the same replicate were paired with males. The number of adult pairs for the different amplitude treatments was as follows: ±0°C: 30 (10, 10, and 10 pairs for each of the three replicates); ±4°C: 30 (10, 10, and 10); ±6°C: 29 (10, 9, and 10); ±8°C: 27 (9, 9, and 9); ±10°C: 25 (9, 8, and 8); and ±12°C: 24 (8, 8, and 8). The pairs were transferred to glass tubes (3 × 12 cm) for mating and oviposition. Nylon mesh (200 μm) was attached to both ends of the glass tube, and cotton balls (immersed in 10% honey–water solution) were placed within the tube for feeding. From 15:00 to 16:00, egg cards (3 × 4 cm sealing film soaked in cabbage juice) were placed in the glass tubes for collecting eggs. The glass tube, egg card, and cotton ball were replaced daily at 08:00 until the adults had died. An adult was considered to have died naturally when no movement was elicited in response to gently touching the body or antennae with a brush. By analyzing the development and survival of eggs laid each day, the interaction of maternal temperature, offspring temperature, and delayed effect on eggs can be determined. The total number of eggs laid each day was recorded, and eggs laid on the first, second, and third days were randomly selected for each temperature treatment. Under each temperature amplitude, 20 eggs of the same size were randomly selected, with the process being repeated three times. In total, 1080 eggs were thus selected (3 d × 6 temperature amplitudes × 3 repeats × 20 eggs). The eggs were placed in sterilized Petri dishes lined with filter paper, to which, 5 ml of sterilized distilled water had been added to maintain a 40–60% RH, and these were placed in the feeding room. The development and survival of eggs were monitored daily at 08:00 until they had either hatched or died. Eggs that failed to hatch and turned black were considered to have died. The entire experiment was conducted over a period of approximately 1 mo from early December 2018 to early January 2019. Statistical Analysis The effects of different temperature amplitudes on the development, survival, longevity, and reproduction of diamondback moths were analyzed using single factor variance (temperature and sex were fixed factors, and repetition was a random factor). Development periods (d) of the different stages were estimated for individuals still alive when entering the next stage, and the reciprocal of the development period (1/d) was the development rate. Longevity was the number of days an adult survived. Adults who were unable to mate, escaped, or died unnaturally were not included. Reproduction refers to the total number of eggs laid by the adult, the incubation rate is the number of larvae/number of eggs × 100%, the pupal rate is the number of pupae/number of larvae × 100%, and the emergence rate is the number of adults/number of pupae × 100%. The development rate was the pupal weight/larva development duration. The percentage of ovipositing in the first three days is the number of ovipositing in the first three days/total ovipositing × 100%. Life table parameters, consisting of the intrinsic rate of increase (rm), net reproductive rate (R0), finite rate of increase (λ), and doubling time (DT) were analyzed according to the age-stage, two-sex life table theory (Chi & Liu, 1985) as described by Chi (Chi, 1988). TWOSEX-MS Chart Visual BASIC (version 6, service pack 6) for Windows (available at http://140.120.197.173/Ecology/ (Chung Hsing University) and http://nhsbig.inhs.uiuc.edu.tw/www/chi.html (Illinois Natural History Survey) were used to analyze the age-stage, two-sex life table data (Chi, H. TWOSEX-MS Chart: a computer program for the age-stage, two-sex life table analysis (http://140.20.197.173/Ecology/Download/Twosex-MSChart.rar, 2013) (Chi, 2020). Means were compared using Tukey’s HSD test. Tukey’s HSD pairwise comparisons of all indexes were conducted using IBM SPSS Statistics Version 20.0. Means were separated using Tukey’s HSD (honestly significant difference) test when significant differences were found at P < 0.05 and were denoted as the means ± SD (standard deviation). All data were analyzed using SPSS 21.0 (SPSS Inc., Chicago, Illinois, USA). To consider the effects of temperature amplitudes during the pupal stage on the development rate of pupae, we compared our results to reported development models (Degree day model, Logistic model, and Wang model) for Plutella xylostella (Lepidoptera: Plutellidae). We found that the Logistic model provided the best fit with our data, and we, therefore, compared our results to predictions based on this model using the parameters in Liu et al. (2002). Since the upper temperature of the development of pupae is 32°C, when the temperature exceeds 32°C, the development of pupae will stop. The development was denoted as zero when hourly temperatures exceeded 32°C (Liu et al. 2002). Results Temperature amplitude (F = 7.16, df = 5, P = 0.004) and gender (F = 881.32, df = 1, P = 0.001) significantly affected pupal development (Table 1). The development rate of pupae at 25°C (0.30 1/d) and moderate temperature amplitudes (rates at ±4, ±6, and ±8°C were 0.30 1/d, 0.29 1/d, 0.27 1/d, respectively) were faster than that at wide temperature amplitudes (rates at ±10 and ±12°C were 0.24 1/d, and 0.20 1/d respectively) (Fig. 1A). When the observed experimental values were compared with the predicted values based on the constant temperature, a logistic model revealed that the observed experimental development rate was faster than predicted for the ±8, ±10, and ±12°C groups. Table 1. Results of ANOVAs for effects of pupal temperatures, sex, and replicate plates (as a random factor, nested within pupal temperatures) on the development rate of pupa, emergence rate, longevity, fecundity, and proportion of females ovipositing in the first three days, in Plutella xylostella Trait . Source . df . F . P . Development rate of pupa Pupa treatment (PT) 5,344 7.16 0.004 Sex (S) 1,344 881.32 0.001 PT × S 5,344 3.42 0.046 Emergence rate Pupa treatment (PT) 5,18 10.00 0.001 Longevity Pupa treatment (PT) 5,333 1.69 0.225 Sex (S) 1,333 432.01 0.002 PT × S 5,333 2.77 0.080 Fecundity Pupa treatment (PT) 5,166 10.82 0.001 Proportional of females ovipositing in the first three days Pupa treatment (PT) 5,166 6.21 0.007 Trait . Source . df . F . P . Development rate of pupa Pupa treatment (PT) 5,344 7.16 0.004 Sex (S) 1,344 881.32 0.001 PT × S 5,344 3.42 0.046 Emergence rate Pupa treatment (PT) 5,18 10.00 0.001 Longevity Pupa treatment (PT) 5,333 1.69 0.225 Sex (S) 1,333 432.01 0.002 PT × S 5,333 2.77 0.080 Fecundity Pupa treatment (PT) 5,166 10.82 0.001 Proportional of females ovipositing in the first three days Pupa treatment (PT) 5,166 6.21 0.007 Significant P—values are given in bold. Open in new tab Table 1. Results of ANOVAs for effects of pupal temperatures, sex, and replicate plates (as a random factor, nested within pupal temperatures) on the development rate of pupa, emergence rate, longevity, fecundity, and proportion of females ovipositing in the first three days, in Plutella xylostella Trait . Source . df . F . P . Development rate of pupa Pupa treatment (PT) 5,344 7.16 0.004 Sex (S) 1,344 881.32 0.001 PT × S 5,344 3.42 0.046 Emergence rate Pupa treatment (PT) 5,18 10.00 0.001 Longevity Pupa treatment (PT) 5,333 1.69 0.225 Sex (S) 1,333 432.01 0.002 PT × S 5,333 2.77 0.080 Fecundity Pupa treatment (PT) 5,166 10.82 0.001 Proportional of females ovipositing in the first three days Pupa treatment (PT) 5,166 6.21 0.007 Trait . Source . df . F . P . Development rate of pupa Pupa treatment (PT) 5,344 7.16 0.004 Sex (S) 1,344 881.32 0.001 PT × S 5,344 3.42 0.046 Emergence rate Pupa treatment (PT) 5,18 10.00 0.001 Longevity Pupa treatment (PT) 5,333 1.69 0.225 Sex (S) 1,333 432.01 0.002 PT × S 5,333 2.77 0.080 Fecundity Pupa treatment (PT) 5,166 10.82 0.001 Proportional of females ovipositing in the first three days Pupa treatment (PT) 5,166 6.21 0.007 Significant P—values are given in bold. Open in new tab Fig. 1. Open in new tabDownload slide (A) Development rate (1/d) of different temperature amplitudes (bottom bar indicates amplitudes) and constant temperature models (x-axis in degree hours). The dotted line and shaded symbols indicate means from the experimental data, the solid line and symbols are the Logistic model describing development rates in diamondback moth based on constant temperature data from Liu et al. (2002). The reciprocal of the development period (1/d) of pupa is the development rate of pupa. (B) Emergence rate under the six different temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Different letters at the top of columns indicate significant differences among treatments at P = 0.05. Fig. 1. Open in new tabDownload slide (A) Development rate (1/d) of different temperature amplitudes (bottom bar indicates amplitudes) and constant temperature models (x-axis in degree hours). The dotted line and shaded symbols indicate means from the experimental data, the solid line and symbols are the Logistic model describing development rates in diamondback moth based on constant temperature data from Liu et al. (2002). The reciprocal of the development period (1/d) of pupa is the development rate of pupa. (B) Emergence rate under the six different temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Different letters at the top of columns indicate significant differences among treatments at P = 0.05. Temperature amplitude had a significant effect on emergence rate (F = 10.00, df = 5, P = 0.001) (Table 1). Compared with wide temperature amplitudes (±10 and ±12°C), constant temperature (25°C) and moderate temperature amplitudes (±4, ±6, and ±8°C) increased emergence by at least 6.9% (Fig. 1B). Temperature amplitude (F = 1.69, df = 5, P = 0.225) had no significant effect on adult longevity, but gender did (F = 432.01, df = 1, P = 0.002) (Table 1, Fig. 2A). Temperature amplitude had a significant effect on female oviposition (F = 10.83, df = 5, P = 0.001) (Table 1). However, compared with a constant temperature of 25°C (157.3 eggs/female), reproduction at wide temperature amplitudes (±10 and ±12°C) decreased by at least 19.2 eggs/female (Fig. 2B). In addition, temperature and amplitude had a significant effect on the proportion of females ovipositing on the first three days (F = 6.22, df = 5, P = 0.007) (Table 1). Compared with the constant temperature at 25°C (68.2%) or moderate temperature amplitudes (±4 and ±6°C were 67.8% and 66.3%, respectively), the proportion of females ovipositing on the first three days increased by 71.8%, 73.9%, and 73.6% at ±8, ±10, and ±12°C, respectively (Fig. 2C), and the proportion of females ovipositing on the first three days increased gradually as the temperature range expanded. Fig. 2. Open in new tabDownload slide Means for (A) longevity, (B) fecundity, and (C) proportion of females ovipositing in first three days under six different temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Different letters at the top of columns indicate significant differences among treatments at P = 0.05. Fig. 2. Open in new tabDownload slide Means for (A) longevity, (B) fecundity, and (C) proportion of females ovipositing in first three days under six different temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Different letters at the top of columns indicate significant differences among treatments at P = 0.05. The life table parameter analysis showed that the intrinsic rate of increase (F = 7.19, df = 5, P = 0.003) and the net reproductive rate (F = 10.52, df = 5, P < 0.001) were significantly affected by temperature amplitude (Table 2). Compared with the constant temperature (25°C) and the moderate temperature amplitudes (±4, ±6, and ±8°C), the intrinsic rate of increase and the net reproductive rate were significantly lower under the widest temperature amplitude (±12°C) (Fig. 3). In addition, the doubling time (F = 7.24, df = 5, P = 0.002) and the finite rate of increase (F = 6.33, df = 5, P = 0.004) were significantly affected by the temperature amplitude (Table 2). Table 2. Life table parameters of Plutella xylostella under different temperature amplitudes with the same mean temperature 25°C Temperature amplitudes (±°C) . λ . R0 . rm . DT . 0 2. 31 ± 0.08 78. 58 ± 1.98 0. 84 ± 0.03 5. 21 ± 0.20 4 2. 40 ± 0.16 76. 98 ± 1.52 0. 87 ± 0.07 4. 99 ± 0.42 6 2. 32 ± 0.13 81. 38 ± 3.86 0. 84 ± 0.06 5. 23 ± 0.29 8 2. 41 ± 0.19 78. 61 ± 3.76 0. 88 ± 0.08 5. 00 ± 0.49 10 2. 11 ± 0.05 71. 42 ± 1.06 0. 75 ± 0.02 5. 72 ± 0.21 12 1. 97 ± 0.02 69. 20 ± 1.23 0. 68 ± 0.01 6. 23 ± 0.06 df 5,18 5,18 5,18 5,18 F 6.33 10.52 7.19 7.24 P 0.004 <0.001 0.003 0.002 Temperature amplitudes (±°C) . λ . R0 . rm . DT . 0 2. 31 ± 0.08 78. 58 ± 1.98 0. 84 ± 0.03 5. 21 ± 0.20 4 2. 40 ± 0.16 76. 98 ± 1.52 0. 87 ± 0.07 4. 99 ± 0.42 6 2. 32 ± 0.13 81. 38 ± 3.86 0. 84 ± 0.06 5. 23 ± 0.29 8 2. 41 ± 0.19 78. 61 ± 3.76 0. 88 ± 0.08 5. 00 ± 0.49 10 2. 11 ± 0.05 71. 42 ± 1.06 0. 75 ± 0.02 5. 72 ± 0.21 12 1. 97 ± 0.02 69. 20 ± 1.23 0. 68 ± 0.01 6. 23 ± 0.06 df 5,18 5,18 5,18 5,18 F 6.33 10.52 7.19 7.24 P 0.004 <0.001 0.003 0.002 Note: rm, intrinsic rate of increase; Ro, net reproductive rate; λ, finite rate of increase; DT, doubling time. X ± SD represents averages and their standard errors respectively. Significant P—values are given in bold. Open in new tab Table 2. Life table parameters of Plutella xylostella under different temperature amplitudes with the same mean temperature 25°C Temperature amplitudes (±°C) . λ . R0 . rm . DT . 0 2. 31 ± 0.08 78. 58 ± 1.98 0. 84 ± 0.03 5. 21 ± 0.20 4 2. 40 ± 0.16 76. 98 ± 1.52 0. 87 ± 0.07 4. 99 ± 0.42 6 2. 32 ± 0.13 81. 38 ± 3.86 0. 84 ± 0.06 5. 23 ± 0.29 8 2. 41 ± 0.19 78. 61 ± 3.76 0. 88 ± 0.08 5. 00 ± 0.49 10 2. 11 ± 0.05 71. 42 ± 1.06 0. 75 ± 0.02 5. 72 ± 0.21 12 1. 97 ± 0.02 69. 20 ± 1.23 0. 68 ± 0.01 6. 23 ± 0.06 df 5,18 5,18 5,18 5,18 F 6.33 10.52 7.19 7.24 P 0.004 <0.001 0.003 0.002 Temperature amplitudes (±°C) . λ . R0 . rm . DT . 0 2. 31 ± 0.08 78. 58 ± 1.98 0. 84 ± 0.03 5. 21 ± 0.20 4 2. 40 ± 0.16 76. 98 ± 1.52 0. 87 ± 0.07 4. 99 ± 0.42 6 2. 32 ± 0.13 81. 38 ± 3.86 0. 84 ± 0.06 5. 23 ± 0.29 8 2. 41 ± 0.19 78. 61 ± 3.76 0. 88 ± 0.08 5. 00 ± 0.49 10 2. 11 ± 0.05 71. 42 ± 1.06 0. 75 ± 0.02 5. 72 ± 0.21 12 1. 97 ± 0.02 69. 20 ± 1.23 0. 68 ± 0.01 6. 23 ± 0.06 df 5,18 5,18 5,18 5,18 F 6.33 10.52 7.19 7.24 P 0.004 <0.001 0.003 0.002 Note: rm, intrinsic rate of increase; Ro, net reproductive rate; λ, finite rate of increase; DT, doubling time. X ± SD represents averages and their standard errors respectively. Significant P—values are given in bold. Open in new tab Fig. 3. Open in new tabDownload slide Mean intrinsic rate of population increase (rm) of Plutella xylostella at six different temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Different letters at the tops of columns indicate significant differences among treatments at P = 0.05. Fig. 3. Open in new tabDownload slide Mean intrinsic rate of population increase (rm) of Plutella xylostella at six different temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Different letters at the tops of columns indicate significant differences among treatments at P = 0.05. Temperature amplitude had a significant effect on egg development on the first day (F = 3.79, df = 5, P = 0.035) (Table 3). Egg development duration increased by at least 0.6 d under the widest temperature amplitude (±12°C) compared with that of other amplitudes (Fig. 4A). Egg development on the second and third days (F = 0.22, df = 5, P = 0.944; F = 0.96, df = 5, P = 0.488) was not significantly affected (Table 3, Figs. 5A and 6A). Table 3. Results of ANOVAs for effects of pupal temperatures and replicate plates (as a random factor, nested within pupal temperatures) on the development times and hatching rates of eggs on the first, second, and third day in Plutella xylostella Trait . Source . df . F . P . Development time of egg on the first day Pupa treatment (PT) 5,306 3.79 0.035 Hatching rate of egg on the first day Pupa treatment (PT) 5,18 2.31 0.109 Development time of egg on the second day Larva treatment (LT) 5,311 0.22 0.944 Hatching rate of egg on the second day Pupa treatment (PT) 5,18 2.45 0.094 Development time of egg on the third day Pupa treatment (PT) 5,319 0.96 0.488 Hatching rate of egg on the third day Pupa treatment (PT) 5,18 1.11 0.404 Trait . Source . df . F . P . Development time of egg on the first day Pupa treatment (PT) 5,306 3.79 0.035 Hatching rate of egg on the first day Pupa treatment (PT) 5,18 2.31 0.109 Development time of egg on the second day Larva treatment (LT) 5,311 0.22 0.944 Hatching rate of egg on the second day Pupa treatment (PT) 5,18 2.45 0.094 Development time of egg on the third day Pupa treatment (PT) 5,319 0.96 0.488 Hatching rate of egg on the third day Pupa treatment (PT) 5,18 1.11 0.404 Significant P—values are given in bold. Open in new tab Table 3. Results of ANOVAs for effects of pupal temperatures and replicate plates (as a random factor, nested within pupal temperatures) on the development times and hatching rates of eggs on the first, second, and third day in Plutella xylostella Trait . Source . df . F . P . Development time of egg on the first day Pupa treatment (PT) 5,306 3.79 0.035 Hatching rate of egg on the first day Pupa treatment (PT) 5,18 2.31 0.109 Development time of egg on the second day Larva treatment (LT) 5,311 0.22 0.944 Hatching rate of egg on the second day Pupa treatment (PT) 5,18 2.45 0.094 Development time of egg on the third day Pupa treatment (PT) 5,319 0.96 0.488 Hatching rate of egg on the third day Pupa treatment (PT) 5,18 1.11 0.404 Trait . Source . df . F . P . Development time of egg on the first day Pupa treatment (PT) 5,306 3.79 0.035 Hatching rate of egg on the first day Pupa treatment (PT) 5,18 2.31 0.109 Development time of egg on the second day Larva treatment (LT) 5,311 0.22 0.944 Hatching rate of egg on the second day Pupa treatment (PT) 5,18 2.45 0.094 Development time of egg on the third day Pupa treatment (PT) 5,319 0.96 0.488 Hatching rate of egg on the third day Pupa treatment (PT) 5,18 1.11 0.404 Significant P—values are given in bold. Open in new tab Fig. 4. Open in new tabDownload slide Means for (A) development time of egg on the first day and (B) hatching rate of egg on the first day under six different temperature amplitudes (±0, ±4, ±6, ±8, ±10 and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Different letters at the top of columns indicate significant differences among treatments at P = 0.05. Fig. 4. Open in new tabDownload slide Means for (A) development time of egg on the first day and (B) hatching rate of egg on the first day under six different temperature amplitudes (±0, ±4, ±6, ±8, ±10 and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Different letters at the top of columns indicate significant differences among treatments at P = 0.05. Fig. 5. Open in new tabDownload slide Means for (A) development time of egg on the second day and (B) hatching rate of egg on the second day under six different temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Fig. 5. Open in new tabDownload slide Means for (A) development time of egg on the second day and (B) hatching rate of egg on the second day under six different temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Fig. 6. Open in new tabDownload slide Means for (A) development time of egg on the third day and (B) hatching rate of egg on the third day under six different temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Fig. 6. Open in new tabDownload slide Means for (A) development time of egg on the third day and (B) hatching rate of egg on the third day under six different temperature amplitudes (±0, ±4, ±6, ±8, ±10, and ±12°C) with the same mean temperature 25°C. Vertical bars indicate ± SD. Temperature amplitude had no significant effect on the egg hatching rate on the first day (F = 2.31, df = 5, P = 0.109) (Table 3). However, with the increase in temperature amplitude, the hatching rate on the first day decreased gradually (Fig. 4B). Temperature amplitude also had no significant effect on the hatching rate on the second and third days (F = 2.45, df = 5, P = 0.094; F = 1.11, df = 5, P = 0.404) (Table 3, Figs. 5B and 6B). Discussion Immediate Effect of Temperature Amplitude Temperature amplitude inhibited the development of pupae under constant temperature (25°C) and moderate temperature amplitudes (±4, ±6, and ±8°C), compared with wide temperature amplitudes (±10 and ±12°C). In accordance with the Kaufman effect (Worner 1992), within an optimum temperature amplitude, insect development shows a linear pattern. The developmental effects of daytime temperatures above the average were equal to those of nighttime temperatures under the average, i.e., they canceled each other out (Zhao et al., 2014) and there was no significant effect on development (Xing et al. 2014, Colinet et al. 2015). Under wide temperature amplitudes (±10 and ±12°C), the highest temperature was higher than the upper limit for pupal development (32°C) (Chen and Liu 2003, Golizadeh et al. 2007). At temperatures of 35–37°C for 6 h, the development of pupae may be inhibited. It is worth noting that the development rate at wide temperature amplitudes was significantly higher than those predicted from the logistic model based on constant temperature, which sets the development rate as zero at temperatures higher than the upper limits for constant temperature. Pupal development still proceeded slowly at the wide temperature amplitudes and did not stop completely. This may be due to recovery from heat injury during optimum nighttime or that damage was not so severe as to affect development. This phenomenon also exists at the larval stage (Xing et al. 2019). Temperature amplitude had little effect on the emergence rate. Previous studies have shown no significant change in the emergence rate of diamondback moths at constant temperatures between 12 and 30°C (98.7–90%), but emergence dropped to 73% at 32°C, and pupae did not survive at 34°C (Chen and Liu 2003). However, our results showed that the emergence rate remained high (70%) under the wide temperature amplitudes (±10 and ±12°C), and the daily maximum of 37°C was far above the reported upper lethal limit for pupae (32°C) (Chen and Liu 2003, Golizadeh et al. 2007). This finding may be due to an increase in protective factors such as HSP protein, mannitol, or sorbitol during the mild nights (Zerebecki and Sorte 2011) and the repair of thermal damage from daytime high temperatures during the night (Yang and Stamp 1995, Zhao et al. 2014). Carry-Over Effects of Temperature Amplitude The wide temperature amplitudes inhibited the total reproduction of the diamondback moth. Although wide temperature amplitudes (±10 and ±12°C) had no significant effect on emergence and adult longevity compared with those from the constant temperature treatment, a significant decrease in adult reproduction was observed. This is consistent with the results of previous studies, which showed that reproductive traits are more sensitive to high temperatures than survival traits (Zhang et al. 2015a, Zhao et al. 2017). Studies have shown that exposure to environmental stress such as malnutrition (Dmitriew and Rowe 2007, Block and Stoks 2008b), temperature (Orizaola et al. 2010, Potter et al. 2011), and oxygen stress (Block and Stoks 2008a) at a certain developmental stage, can directly affect survival, development, reproduction, and other traits. This may be due to the redistribution of energy in the body after a certain developmental stage (Metcalfe and Monaghan 2001). For example, heat shock induces the body to produce heat shock proteins (Gu et al. 2012), which consume more energy in the body (Tomanek and Zuzow 2010) and, in turn, affect reproduction in subsequent developmental stages. On the other hand, the wide temperature amplitudes during the pupal stage significantly increased the number of eggs in the early stage. The proportion of females ovipositing on the first three days was significantly higher (up to 73.6%) in the highest temperature amplitude (±12°C) condition than under constant temperature or moderate temperature amplitudes (±4 and ±6°C were 66.2% and 68.2%, respectively). Studies have shown that environmental stress can induce adults to lay eggs as early as possible to avoid adverse effects on subsequent life stages (Javoiš and Tammaru 2004, Zhang et al. 2015b). In the experiment, under adverse conditions (daily temperature of 35°C under the wide temperature amplitude ±10°C), individual fitness reached a maximum as soon as possible before death, by accelerating ovipositing; this may be an adaptive response to environmental stress. Transgenerational Effects of Temperature Amplitude The wide temperature amplitudes influenced both the development and survival of offspring. The pupae experienced a wide temperature amplitude (±12°C), which significantly inhibited egg development and reduced the hatching rate on the first day but had no effect on the development or survival of the eggs on the second or third days. Studies have shown that temperature has a transgenerational effect on the expression of fitness-related traits (Walsh et al. 2014). For example, the environmental temperature in the parent generation affects the size, survival, development, thermal tolerance, and flight ability of offspring (Stillwell and Fox 2005, Ismaeil et al. 2013, Ferrer et al. 2013, Macagno et al. 2018). The ovarian development and egg maturation of the diamondback moth begin in the pupal stage, and there are many mature eggs in the ovaries of new adults (Liang et al. 2019). When pupae experience wide temperature amplitudes (±10 and 12°C), the heat shock reaction leads to the parent consuming more energy, which may lead to the reduced early yolk and chorionic membrane formation (Sørensen et al. 2005). This could then lead to a reduction in the distribution of egg nutrients, which has an impact on the development and survival of eggs on the first day. The reason why there was no significant change in the development and survival of eggs on the second and third day may be because these eggs did not complete their development until after the emergence of the adult. At this time, the environment had returned to the normal feeding temperature, the ovaries were not affected by the high temperature, and the eggs obtained sufficient nutrients during development. Pest Management Implications In the past, dynamic projections for insect populations have mainly been based on predictive models using average temperatures (Cocuzza et al. 1997, Stevens 2003, Garcia et al. 2009, Aminatou et al. 2011). However, different temperature amplitudes around the same average temperature had a significant effect on diamondback moth populations. In low latitude areas such as Wuhan, the diurnal temperature amplitude is below ± 6°C at which, the development of DBM can hardly be influenced and is similar to that at a constant temperature. However, in high latitude areas such as Beijing, the diurnal temperature amplitude is above ± 8°C at which, the development of DBM may be restricted and is slower than at constant temperature, and the intrinsic growth rate significantly decreased (Fig. 3). In addition, pupae that experienced different temperature amplitudes showed significant changes in their development and reproduction, and effects were seen in the development and survival of their offspring. From these results, we can conclude that different temperature amplitudes around the same average temperature must be considered in population dynamics models, to accurately simulate the effects of complex natural temperature patterns on the population ecology of diamondback moths. Such models would facilitate predictions of field occurrence, which has practical implications for farmers of cruciferous vegetables. Acknowledgments We thank Chen Kang for assistance in completing experiments. This work was funded by the Natural Science Foundation of Shanxi Province (201701D121113, 2015011075), the Foundation in Shanxi Academy of Agricultural Sciences (YBSJJ1703, YBSJJ1512, YYDZX16, and YCX2018D2BH5) and the Province Key Research and Development Program of Shanxi (201903D211001-2). 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TI - Within- and Trans-Generational Life History Responses to Diurnal Temperature Amplitudes of the Pupal Stage in the Diamondback Moth
JF - Environmental Entomology
DO - 10.1093/ee/nvab044
DA - 2021-05-11
UR - https://www.deepdyve.com/lp/oxford-university-press/within-and-trans-generational-life-history-responses-to-diurnal-lL7Hynzpyt
SP - 1
EP - 1
VL - Advance Article
IS - 
DP - DeepDyve
ER -