TY - JOUR
AU1 - Shi,, Meng-Zhu
AU2 - Li,, Jian-Yu
AU3 - Ding,, Bo
AU4 - Fu,, Jian-Wei
AU5 - Zheng,, Li-Zhen
AU6 - Chi,, Hsin
AB - Abstract Alligatorweed, Alternanthera philoxeroide (Mart.) Griseb. (Amaranthaceae) is an invasive weed in China that is often kept under control by the alligatorweed flea beetle, Agasicles hygrophila Selman and Vogt (Coleoptera: Chrysomelidae) introduced into China from Argentina in the 1980s. Elevated CO2 levels have been shown to have a direct effect on Ag. hygrophila. In order to fully evaluate the indirect effects of three different atmospheric concentrations of CO2 (420, 550, and 750 ppm) on the population parameters of Ag. hygrophila reared on Al. philoxeroides, we collected life table data for Ag. hygrophila using the age-stage, two-sex life table method. In general, there were no significant differences in the lengths of the preadult parameters among the three treatments. The adult duration and total longevity of males, however, did increase as CO2 increased in concentration. Although the adult preoviposition and total preoviposition periods decreased, the fecundity, oviposition days, eggs per oviposition day, net reproductive rate, intrinsic rate of increase, and finite rate of increase all increased significantly at the high CO2 concentration. Consequently, we determined that the Ag. hygrophila population size will potentially increase rapidly over a short period of time at elevated CO2 concentrations. Our results suggest that 550 and 750 ppm CO2 may also cause physiological changes in Al. philoxeroides that, in turn, provide enhanced nutrition for increasing reproduction in Ag. hygrophila by accelerating maturation of their reproductive system. These results indicate that the efficacy of Ag. hygrophila as a biological control agent against Al. philoxeroides will likely be increased at 550 and 750 ppm CO2. Agasicles hygrophila, Alternanthera philoxeroides, elevated CO2, two-sex life table, indirect effect Alligatorweed, Alternanthera philoxeroides (Mart.) Griseb. (Amaranthaceae), is an important, invasive, aquatic weed originating from the Parana River region of South America (Vogt et al. 1979) that has subsequently been introduced into many countries. Following its introduction into China in the 1930s, Al. philoxeroides has spread rapidly through 16 provinces, and is now extensively distributed between latitudes 18° and 35° North and longitudes 100° and 121° East (Ma 2001). In 2003, Al. philoxeroides was listed as one of the 16 most important alien invasive species by China’s Ministry of Environmental Protection (MEP and CAS 2003). The primary biological control agent that has been successfully used against Al. philoxeroides in Australia is the flea beetle, Agasicles hygrophila Selman and Vogt (Coleoptera: Chrysomelidae) (Sainty et al. 1998). In 1986, this agent was introduced into China and was found to be effective in the control of populations of Al. philoxeroides within that country (Ma 2001). The larval and adult flea beetles feed directly on the emergent foliage of Al. philoxeroides; afterward, the mature larvae bore into the hollow stems in which they subsequently pupate. Their burrowing weakens the plant stems, eventually leading to their collapse (Lu et al. 2010). A major factor likely to affect the efficacy of pest management measures is climate change and associated environmental changes, including increases in the levels of greenhouse gases. Concentrations of the principal greenhouse gases, carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O), have been increasing in the atmosphere since 1750 owing to human activities (Stocker et al. 2014). Of these, CO2 is responsible for 50–60% of global warming (Fuwa 1994). In 2011, the atmospheric concentration of 391 ppm CO2 exceeded preindustrial levels by approximately 40%, and is predicted to increase to 550 ppm by the year 2050 and 770 ppm by 2200 (Solomon et al. 2007). A number of studies have shown that elevated levels of CO2 have considerable effects on various species of the fauna and flora, including plants (Huang et al. 2017, Mateos-Naranjo et al. 2010), insects (Chen et al. 2005, Shi et al. 2014), and aquatic organisms (Parra et al. 2016). Some of these reports have demonstrated that these effects may often be indirect. For example, it has been shown that the direct effects of elevated CO2 on the cotton bollworm Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) are weak (Yin et al. 2010) and that it mainly affects these insects indirectly via a cascade effect through their plant hosts (Wu et al. 2006, Sun et al. 2011). Assessment of the direct effects of elevated CO2 via an examination of the life table and population dynamics of Ag. hygrophila has shown that the intrinsic rate of increase (r), finite rate of increase (λ), and net reproduction rate (R0) are higher, and that the mean generation time (T) is shorter under 750 µl/liter CO2 than it is at ambient CO2 conditions (420 µl/liter) (Fu et al. 2016). In the present study, we assessed the indirect effect of elevated CO2 on Ag. hygrophila when the host plant, Al. philoxeroides, was initially cultivated under three different concentrations of CO2 (420, 550, and 750 ppm) and then used to rear the beetles. The objectives of this study were to 1) determine the changes, if any, in the population parameters of Ag. hygrophila reared on Al. philoxeroides that had been cultivated under different CO2 conditions, 2) compare the life table parameters, using the comprehensive age-stage, two-sex life table theory, with values reported in previous life table studies (Fu et al. 2016), and 3) predict the population growth of Ag. hygrophila and its potential for the control of Al. philoxeroides under conditions of increasing CO2 concentrations. Materials and Methods Closed-Dynamics CO2 Chambers All experiments were conducted in growth chambers (PRX-450D; Haishu Safe Apparatus, Ningbo, China) under controlled environmental conditions, i.e., a photoperiod of 14:10 (L:D) h, temperatures of 26 ± 1°C during the light period and 24 ± 1°C during the dark period, and relative humidity (RH) of 75 ± 5%. Three CO2 concentrations were used in this study: 420 ± 20.1 ppm (ambient CO2 condition), 550 ± 24.4 ppm, and 750 ± 28.8 ppm. The CO2 concentrations in the growth chambers were maintained using CO2 controllers designed by the Institute of Plant Protection, Fujian Academy of Agricultural Sciences (IPP, FAAS), Fujian Province, and constructed by Foshan Shunyidong Electronic Science & Technology Co. Ltd, Guangdong Province, China (new pattern patent No. ZL 201320567450.X). The controllers continuously monitored CO2 concentrations and recorded the generated data. At the end of the experiment, the CO2 concentration data were exported, and the mean averages were calculated. Cultivation of Al. philoxeroides Al. philoxeroides, originally collected from a river in Nantong Town, Minhou County, Fuzhou, China, was grown in a greenhouse at IPP, FAAS. For the purposes of this study, Al. philoxeroides plants were propagated from stem cuttings. Stems of approximately 5 cm in length with a single node were inserted into planting soil in pots (length: 47.5 cm, width: 34 cm, height: 15 cm). The pots were kept in growth chambers under one of the three CO2 conditions for 30 d. Plants 20–30 cm high were used in the experiments. Rearing of Ag. hygrophila Ag. hygrophila colonies were originally collected from an experimental field at the IPP, FAAS and reared in a growth chamber at 25 ± 1°C, 75% ± 5% RH, and a photoperiod of 14:10 (L:D) h. In this study, different treatment groups of Ag. hygrophila were reared under ambient CO2 condition on Al. philoxeroides grown under one of the three CO2 conditions described earlier. Egg masses laid on leaves within a 24-h period were randomly selected and transferred to glass Petri dishes (diameter: 11 cm). After eclosion, the first instar larvae were transferred to a fresh glass Petri dish (diameter: 9 cm) containing a premoistened filter paper and reared individually. The larvae were supplied with fresh Al. philoxeroides leaves as needed until pupation. A section of Al. philoxeroides tip consisting of two stem nodes (length: 4–5 cm) without leaves was provided for pupation. Newly emerged adult males and females were paired and maintained in individual glass rearing containers (diameter: 5 cm, height: 8 cm) for oviposition. When there was an excess of one sex or one of the paired beetles died earlier than its mate, they were paired with adults of the opposite sex from the colonies mass-reared on Al. philoxeroides grown under the same CO2 concentration. The hatching, development, survival, and fecundity of each beetle were recorded daily until the death of all individuals. Life Table Data Analysis The life history data of Ag. hygrophila, including developmental duration, lifespan, female daily fecundity, life expectancy, and population parameters, were analyzed using the program TWOSEX-MSChart (Chi 2018b) based on the theory of the age-stage, two-sex life table described by Chi and Liu (1985) and Chi (1988). According to Mou et al. (2015) and Chi et al. (2016), any egg batch sampled for life table study will differentially influence the population parameters by its hatch rate. Furthermore, they derived a mathematical proof demonstrating the importance of using only the viable, hatched eggs when calculating survival, development data, and daily fecundity to correctly estimate the population parameters. Based on their findings, we used only hatched eggs in the following life table analysis. The age-stage-specific survival rate (sxj, where x = age and j = stage), age-specific survival rate (lx), age-stage-specific fecundity (fxj), age-specific fecundity (mx), and population parameters, including intrinsic rate of increase (r), finite rate of increase (λ), net reproductive rate (R0), and mean generation time (T), were calculated according to Chi and Liu (1985) by using the following equation: lx=∑j=1ksxj (1) where k is the number of stages. mx=∑j=1ksxjfxj∑j=1ksxj (2) The value for r was estimated from the Euler–Lotka equation with age indexed from 0 as follows: ∑x=0∞e−r(x+1)lxmx=1 (3) The finite rate of increase (λ), the net reproductive rate (R0), and the mean generation time (T) were calculated as follows: λ=er (4) R0=∑x=0∞lxmx (5) T=lnR0r (6) The age- and stage-specific life expectancy (exj), which is the length of time an individual of age x and stage j is expected to live, was calculated according to Chi and Su (2006) as follows: exj=∑i=x∞∑y=jks′iy (7) where s′iy is the probability that an individual of age x and stage j will survive to age i and stage y and was calculated by assuming s′xj= 1. Oviposition days (Od) is the mean number of days on which adult females actually lay eggs and was calculated as follows: Od=∑x=1NfrDxNfr (8) where Nfr is the number of reproductive females, i.e., females that laid at least one egg, and Dx is the number of oviposition days of the xth reproductive female (Chen et al. 2018). The number of eggs per oviposition day (Ed) was calculated as follows: Ed=∑x=1NfrEx∑x=1NfrDx=∑x=1NfrExOd×Nfr=FrOd (9) where Ex is the total number of eggs produced by a reproductive female, and Fr is the mean fecundity based on reproductive females (Chen et al. 2018). With reference to Fisher (1993), the age-stage reproductive value (vxj) is defined as the contribution an individual of age x and stage j has to the future population. According to Huang and Chi (2011) and Tuan et al. (2014a, 2014b), vxj in the age-stage, two-sex life table is calculated as follows: vxj=er(x+1)sxj∑i=x∞e−r(i+1)∑y=1ks′iyfiy (10) The variances and standard errors were estimated using the bootstrap method with resampling 100,000 times (Efron and Tibshirani 1993, Huang and Chi 2012). Although the Weibull function has often been used to fit and compare survival curves (lx) of different treatments, Tuan et al. (2017) discussed some of the problems associated with using it. Because the number of surviving individuals usually does not decrease in a consistent manner, the survival rate may decrease from 55% at age x to 48% at age x+1, making it impractical to find the age of an exact survival rate. By using the bootstrap technique, however, an age where a survival rate is lower than a specific percentage (e.g., 50 or 5%) can be accessed and compared without unrealistic assumptions. In this study, we accessed and compared the ages where the survival rate was <50 and <5%. Population Projection Because the intrinsic rate of increase (r) is estimated based on the assumption that a population reaches a stable age-stage structure as time approaches infinity, it is inappropriate to use r to project population growth before that assumption is fulfilled. To predict and compare the population growth and age-stage structure of Ag. hygrophila reared on Al. philoxeroides grown under the three different CO2 concentrations, we used life table data, i.e., the developmental rate, survival rate, and fecundity, to simulate population growth using the program TIMING-MSChart (Chi 2018a). An initial population of 10 newly laid eggs was used for the simulation. Given that age-stage, two-sex life tables can be used to describe stage differentiation during population growth, we calculated the increase rate of stage j from time t to t+1 by using a common logarithm: φj,t=log(nj,t+1+1nj,t+1) (11) where nj,t is the number of individuals in stage j at time t. We also used a natural logarithm to calculate the increase rate of stage j from time t to t+1: rj,t=ln(nj,t+1+1nj,t+1)=ln(nj,t+1+1)−ln(nj,t+1) (12) Because the number of individuals in a stage can be 0 (nj,t = 0 or nj,t+1 = 0), but the logarithm of zero cannot be defined, we used nj,t +1 and nj,t+1+1 in the calculation of φj,t and rj,t (Akca et al. 2015, Huang et al. 2018). Results Age-Stage, Two-Sex Life Tables of Ag. Hygrophila The developmental times of the eggs, first through third instar larvae, and pupae differed under the different CO2 conditions. The developmental times for all stages were significantly different between the 550 ppm and 750 ppm treatments, as was that (with the exception of the first instar larvae) between the ambient CO2 condition (420 ppm) and 550 ppm. However, the total developmental time for the cumulative preadult stages (18.9, 18.6, and 18.9 d at 420, 550, and 750 ppm, respectively) showed no significant difference among the three CO2 treatments. Although we noted prolonged adult male longevity and an extended overall male lifespan at higher CO2 concentrations, no significant differences among treatments were detected for adult female longevity or overall female lifespan. An evident reduction was noted in the adult preoviposition period (APOP) of females reared on Al. philoxeroides grown under high CO2 concentration. The total preoviposition period (TPOP) under ambient CO2 conditions was longer than that under the 550 and 750 ppm CO2 conditions. Moreover, the number of oviposition days (Od), number of eggs per oviposition day (Ed), and female lifetime fecundity, i.e., F (mean fecundity of all females) and Fr (mean fecundity of reproductive females), showed apparent increases with increasing CO2 concentration (Table 1). Table 1. Developmental time, longevity, adult preoviposition period (APOP), total preoviposition period (TPOP), oviposition days (Od), eggs per oviposition day (Ed), fecundity of all females (F), and fecundity of reproductive females (Fr) of Agasicles hygrophila reared on Alternanthera philoxeroides cultivated at three different CO2 concentrations 420 ppm 550 ppm 750 ppm Parameters n Mean ± SE n Mean ± SE n Mean ± SE Egg duration (days) 179 4.1 ± 0.02b 204 4.0 ± 0.01c 239 4.2 ± 0.03a First instar duration (days) 153 3.1 ± 0.02a 171 3.1 ± 0.02a 227 2.9 ± 0.03b Second instar duration (days) 142 2.3 ± 0.03b 161 2.1 ± 0.02c 224 2.4 ± 0.03a Third instar duration (days) 127 2.9 ± 0.05b 143 3.1 ± 0.04a 210 2.7 ± 0.05c Total larval duration (days) 127 8.2 ± 0.06a 143 8.3 ± 0.06a 210 8.0 ± 0.05b Pupal duration (days) 88 6.7 ± 0.09a 104 6.3 ± 0.08b 167 6.7 ± 0.05a Pre-adult duration (days) 88 18.9 ± 0.10a 104 18.6 ± 0.07a 167 18.9 ± 0.05a Adult female duration (days) 45 8.5 ± 0.63a 57 9.4 ± 0.61a 91 10.0 ± 0.52a Adult male duration (days) 43 9.0 ± 0.64b 47 9.3 ± 0.69b 76 11.5 ± 0.75a Overall female life span (days) 45 27.4 ± 0.64a 57 27.9 ± 0.63a 91 28.8 ± 0.53a Overall male life span (days) 43 27.9 ± 0.66b 47 28.0 ± 0.71b 76 30.4 ± 0.74a APOP (days) 28 5.4 ± 0.26a 39 4.5 ± 0.12b 69 3.9 ± 0.08c TPOP (days) 28 24.1 ± 0.26a 39 22.9 ± 0.12b 69 22.7 ± 0.10b Oviposition days (Od; days) 28 1.9 ± 0.27c 39 4.0 ± 0.37b 69 5.4 ± 0.39a Eggs per oviposition day (Ed) (eggs/day) 28 23.2 ± 1.2c 39 29.3 ± 0.9b 69 31.6 ± 0.7a Fecundity (Fr) (eggs/reproductive female) 28 44.7 ± 7.04c 39 115.8 ± 13.15b 69 169.8 ± 12.58a Fecundity (F) (eggs/female) 45 27.8 ± 5.44c 57 79.2 ± 11.49b 91 128.7 ± 12.22a 420 ppm 550 ppm 750 ppm Parameters n Mean ± SE n Mean ± SE n Mean ± SE Egg duration (days) 179 4.1 ± 0.02b 204 4.0 ± 0.01c 239 4.2 ± 0.03a First instar duration (days) 153 3.1 ± 0.02a 171 3.1 ± 0.02a 227 2.9 ± 0.03b Second instar duration (days) 142 2.3 ± 0.03b 161 2.1 ± 0.02c 224 2.4 ± 0.03a Third instar duration (days) 127 2.9 ± 0.05b 143 3.1 ± 0.04a 210 2.7 ± 0.05c Total larval duration (days) 127 8.2 ± 0.06a 143 8.3 ± 0.06a 210 8.0 ± 0.05b Pupal duration (days) 88 6.7 ± 0.09a 104 6.3 ± 0.08b 167 6.7 ± 0.05a Pre-adult duration (days) 88 18.9 ± 0.10a 104 18.6 ± 0.07a 167 18.9 ± 0.05a Adult female duration (days) 45 8.5 ± 0.63a 57 9.4 ± 0.61a 91 10.0 ± 0.52a Adult male duration (days) 43 9.0 ± 0.64b 47 9.3 ± 0.69b 76 11.5 ± 0.75a Overall female life span (days) 45 27.4 ± 0.64a 57 27.9 ± 0.63a 91 28.8 ± 0.53a Overall male life span (days) 43 27.9 ± 0.66b 47 28.0 ± 0.71b 76 30.4 ± 0.74a APOP (days) 28 5.4 ± 0.26a 39 4.5 ± 0.12b 69 3.9 ± 0.08c TPOP (days) 28 24.1 ± 0.26a 39 22.9 ± 0.12b 69 22.7 ± 0.10b Oviposition days (Od; days) 28 1.9 ± 0.27c 39 4.0 ± 0.37b 69 5.4 ± 0.39a Eggs per oviposition day (Ed) (eggs/day) 28 23.2 ± 1.2c 39 29.3 ± 0.9b 69 31.6 ± 0.7a Fecundity (Fr) (eggs/reproductive female) 28 44.7 ± 7.04c 39 115.8 ± 13.15b 69 169.8 ± 12.58a Fecundity (F) (eggs/female) 45 27.8 ± 5.44c 57 79.2 ± 11.49b 91 128.7 ± 12.22a Means in the same row followed by the same letter are not significantly different (P < 0.05), as determined by the paired bootstrap test. Open in new tab Table 1. Developmental time, longevity, adult preoviposition period (APOP), total preoviposition period (TPOP), oviposition days (Od), eggs per oviposition day (Ed), fecundity of all females (F), and fecundity of reproductive females (Fr) of Agasicles hygrophila reared on Alternanthera philoxeroides cultivated at three different CO2 concentrations 420 ppm 550 ppm 750 ppm Parameters n Mean ± SE n Mean ± SE n Mean ± SE Egg duration (days) 179 4.1 ± 0.02b 204 4.0 ± 0.01c 239 4.2 ± 0.03a First instar duration (days) 153 3.1 ± 0.02a 171 3.1 ± 0.02a 227 2.9 ± 0.03b Second instar duration (days) 142 2.3 ± 0.03b 161 2.1 ± 0.02c 224 2.4 ± 0.03a Third instar duration (days) 127 2.9 ± 0.05b 143 3.1 ± 0.04a 210 2.7 ± 0.05c Total larval duration (days) 127 8.2 ± 0.06a 143 8.3 ± 0.06a 210 8.0 ± 0.05b Pupal duration (days) 88 6.7 ± 0.09a 104 6.3 ± 0.08b 167 6.7 ± 0.05a Pre-adult duration (days) 88 18.9 ± 0.10a 104 18.6 ± 0.07a 167 18.9 ± 0.05a Adult female duration (days) 45 8.5 ± 0.63a 57 9.4 ± 0.61a 91 10.0 ± 0.52a Adult male duration (days) 43 9.0 ± 0.64b 47 9.3 ± 0.69b 76 11.5 ± 0.75a Overall female life span (days) 45 27.4 ± 0.64a 57 27.9 ± 0.63a 91 28.8 ± 0.53a Overall male life span (days) 43 27.9 ± 0.66b 47 28.0 ± 0.71b 76 30.4 ± 0.74a APOP (days) 28 5.4 ± 0.26a 39 4.5 ± 0.12b 69 3.9 ± 0.08c TPOP (days) 28 24.1 ± 0.26a 39 22.9 ± 0.12b 69 22.7 ± 0.10b Oviposition days (Od; days) 28 1.9 ± 0.27c 39 4.0 ± 0.37b 69 5.4 ± 0.39a Eggs per oviposition day (Ed) (eggs/day) 28 23.2 ± 1.2c 39 29.3 ± 0.9b 69 31.6 ± 0.7a Fecundity (Fr) (eggs/reproductive female) 28 44.7 ± 7.04c 39 115.8 ± 13.15b 69 169.8 ± 12.58a Fecundity (F) (eggs/female) 45 27.8 ± 5.44c 57 79.2 ± 11.49b 91 128.7 ± 12.22a 420 ppm 550 ppm 750 ppm Parameters n Mean ± SE n Mean ± SE n Mean ± SE Egg duration (days) 179 4.1 ± 0.02b 204 4.0 ± 0.01c 239 4.2 ± 0.03a First instar duration (days) 153 3.1 ± 0.02a 171 3.1 ± 0.02a 227 2.9 ± 0.03b Second instar duration (days) 142 2.3 ± 0.03b 161 2.1 ± 0.02c 224 2.4 ± 0.03a Third instar duration (days) 127 2.9 ± 0.05b 143 3.1 ± 0.04a 210 2.7 ± 0.05c Total larval duration (days) 127 8.2 ± 0.06a 143 8.3 ± 0.06a 210 8.0 ± 0.05b Pupal duration (days) 88 6.7 ± 0.09a 104 6.3 ± 0.08b 167 6.7 ± 0.05a Pre-adult duration (days) 88 18.9 ± 0.10a 104 18.6 ± 0.07a 167 18.9 ± 0.05a Adult female duration (days) 45 8.5 ± 0.63a 57 9.4 ± 0.61a 91 10.0 ± 0.52a Adult male duration (days) 43 9.0 ± 0.64b 47 9.3 ± 0.69b 76 11.5 ± 0.75a Overall female life span (days) 45 27.4 ± 0.64a 57 27.9 ± 0.63a 91 28.8 ± 0.53a Overall male life span (days) 43 27.9 ± 0.66b 47 28.0 ± 0.71b 76 30.4 ± 0.74a APOP (days) 28 5.4 ± 0.26a 39 4.5 ± 0.12b 69 3.9 ± 0.08c TPOP (days) 28 24.1 ± 0.26a 39 22.9 ± 0.12b 69 22.7 ± 0.10b Oviposition days (Od; days) 28 1.9 ± 0.27c 39 4.0 ± 0.37b 69 5.4 ± 0.39a Eggs per oviposition day (Ed) (eggs/day) 28 23.2 ± 1.2c 39 29.3 ± 0.9b 69 31.6 ± 0.7a Fecundity (Fr) (eggs/reproductive female) 28 44.7 ± 7.04c 39 115.8 ± 13.15b 69 169.8 ± 12.58a Fecundity (F) (eggs/female) 45 27.8 ± 5.44c 57 79.2 ± 11.49b 91 128.7 ± 12.22a Means in the same row followed by the same letter are not significantly different (P < 0.05), as determined by the paired bootstrap test. Open in new tab The age-stage-specific survival rate curves (sxj) which demonstrate the survival probability of an egg to age x and stage j, showed stage differentiation and stage overlapping due to the variable developmental time among individuals (Fig. 1). The overall lifespan of male Ag. hygrophila was longer for those individuals reared on Al. philoxeroides grown under 750 ppm CO2 concentration than under 420 ppm and 550 ppm (Fig. 1). The first ages of survival rate <50% and <5% in 750 ppm CO2 treatment were significantly later than those in 550 and 420 ppm (Table 2, Fig. 2). The mx and net maternity (lxmx) tended to increase with increasing CO2 concentration. The highest peak values of lxmx were 2.14 on day 25, 5.11 on day 24, and 8.76 on day 23 for Ag. hygrophila reared on Al. philoxeroides grown under 420, 550, and 750 ppm CO2, respectively (Fig. 2). Although a high peak (20 eggs/individual) was observed on day 37 for the 420 ppm CO2 treatment, the lxmx was low (0.06 eggs/individual) because of the low survival rate at that time. At CO2 concentrations of 420, 550, and 750 ppm, the exj of newly laid eggs were 20.3, 20.3, and 25.1 d, respectively. In general, high peak exj values were observed in the 750 ppm CO2 treatment for each stage, with the life expectancy of adult males being distinctly longer than that of adult females (Fig. 3). The age-stage reproductive values (vxj) of Ag. hygrophila increased with increasing CO2 concentration, with the highest female vxj peaks observed on day 23 (vxj values of 70.17 and 95.04 for 550 and 750 ppm CO2, respectively) (Fig. 4). Table 2. Population parameters and proportions of females, reproductive females, males, and N-type individuals (those that died in preadult stages) of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations CO2 level Population parameters 420 ppm 550 ppm 750 ppm Preadult survival rate (%) 49.2 ± 0.37b 51.0 ± 0.03b 69.9 ± 2.96a First age of survival rate <50% (day) 19.0 ± 1.3b 20.0 ± 1.1b 26.0 ± 0.8a First age of survival rate <5% (day) 35.0 ± 2.2b 35.0 ± 1.7b 39.0 ± 1.2a Net reproductive rate (R0, offspring) 6.99 ± 1.62c 22.11 ± 4.05b 49.02 ± 6.14a Intrinsic rate of increase (r/day) 0.0715 ± 0.0085c 0.1180 ± 0.0067b 0.1476 ± 0.0046a Finite rate of increase (λ/day) 1.0741 ± 0.0091c 1.1253 ± 0.0076b 1.1591 ± 0.0053a Mean generation time (T/day) 26.8 ± 0.50a 26.1 ± 0.30a 26.3 ± 0.23a Proportion of female individuals (Nf/N) 0.251 ± 0.032b 0.279 ± 0.032b 0.381 ± 0.031a Proportion of male individuals (Nm/N) 0.240 ± 0.031ab 0.230 ± 0.030b 0.318 ± 0.030a Proportion of N-type individuals (Nn/N) 0.508 ± 0.037b 0.490 ± 0.035b 0.301 ± 0.030a Proportion of reproductive females (Nfr/Nf) 0.622 ± 0.073a 0.684 ± 0.062a 0.758 ± 0.045a CO2 level Population parameters 420 ppm 550 ppm 750 ppm Preadult survival rate (%) 49.2 ± 0.37b 51.0 ± 0.03b 69.9 ± 2.96a First age of survival rate <50% (day) 19.0 ± 1.3b 20.0 ± 1.1b 26.0 ± 0.8a First age of survival rate <5% (day) 35.0 ± 2.2b 35.0 ± 1.7b 39.0 ± 1.2a Net reproductive rate (R0, offspring) 6.99 ± 1.62c 22.11 ± 4.05b 49.02 ± 6.14a Intrinsic rate of increase (r/day) 0.0715 ± 0.0085c 0.1180 ± 0.0067b 0.1476 ± 0.0046a Finite rate of increase (λ/day) 1.0741 ± 0.0091c 1.1253 ± 0.0076b 1.1591 ± 0.0053a Mean generation time (T/day) 26.8 ± 0.50a 26.1 ± 0.30a 26.3 ± 0.23a Proportion of female individuals (Nf/N) 0.251 ± 0.032b 0.279 ± 0.032b 0.381 ± 0.031a Proportion of male individuals (Nm/N) 0.240 ± 0.031ab 0.230 ± 0.030b 0.318 ± 0.030a Proportion of N-type individuals (Nn/N) 0.508 ± 0.037b 0.490 ± 0.035b 0.301 ± 0.030a Proportion of reproductive females (Nfr/Nf) 0.622 ± 0.073a 0.684 ± 0.062a 0.758 ± 0.045a Means in the same row followed by different letters are significantly different (P < 0.05), as determined by the paired bootstrap test. Open in new tab Table 2. Population parameters and proportions of females, reproductive females, males, and N-type individuals (those that died in preadult stages) of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations CO2 level Population parameters 420 ppm 550 ppm 750 ppm Preadult survival rate (%) 49.2 ± 0.37b 51.0 ± 0.03b 69.9 ± 2.96a First age of survival rate <50% (day) 19.0 ± 1.3b 20.0 ± 1.1b 26.0 ± 0.8a First age of survival rate <5% (day) 35.0 ± 2.2b 35.0 ± 1.7b 39.0 ± 1.2a Net reproductive rate (R0, offspring) 6.99 ± 1.62c 22.11 ± 4.05b 49.02 ± 6.14a Intrinsic rate of increase (r/day) 0.0715 ± 0.0085c 0.1180 ± 0.0067b 0.1476 ± 0.0046a Finite rate of increase (λ/day) 1.0741 ± 0.0091c 1.1253 ± 0.0076b 1.1591 ± 0.0053a Mean generation time (T/day) 26.8 ± 0.50a 26.1 ± 0.30a 26.3 ± 0.23a Proportion of female individuals (Nf/N) 0.251 ± 0.032b 0.279 ± 0.032b 0.381 ± 0.031a Proportion of male individuals (Nm/N) 0.240 ± 0.031ab 0.230 ± 0.030b 0.318 ± 0.030a Proportion of N-type individuals (Nn/N) 0.508 ± 0.037b 0.490 ± 0.035b 0.301 ± 0.030a Proportion of reproductive females (Nfr/Nf) 0.622 ± 0.073a 0.684 ± 0.062a 0.758 ± 0.045a CO2 level Population parameters 420 ppm 550 ppm 750 ppm Preadult survival rate (%) 49.2 ± 0.37b 51.0 ± 0.03b 69.9 ± 2.96a First age of survival rate <50% (day) 19.0 ± 1.3b 20.0 ± 1.1b 26.0 ± 0.8a First age of survival rate <5% (day) 35.0 ± 2.2b 35.0 ± 1.7b 39.0 ± 1.2a Net reproductive rate (R0, offspring) 6.99 ± 1.62c 22.11 ± 4.05b 49.02 ± 6.14a Intrinsic rate of increase (r/day) 0.0715 ± 0.0085c 0.1180 ± 0.0067b 0.1476 ± 0.0046a Finite rate of increase (λ/day) 1.0741 ± 0.0091c 1.1253 ± 0.0076b 1.1591 ± 0.0053a Mean generation time (T/day) 26.8 ± 0.50a 26.1 ± 0.30a 26.3 ± 0.23a Proportion of female individuals (Nf/N) 0.251 ± 0.032b 0.279 ± 0.032b 0.381 ± 0.031a Proportion of male individuals (Nm/N) 0.240 ± 0.031ab 0.230 ± 0.030b 0.318 ± 0.030a Proportion of N-type individuals (Nn/N) 0.508 ± 0.037b 0.490 ± 0.035b 0.301 ± 0.030a Proportion of reproductive females (Nfr/Nf) 0.622 ± 0.073a 0.684 ± 0.062a 0.758 ± 0.045a Means in the same row followed by different letters are significantly different (P < 0.05), as determined by the paired bootstrap test. Open in new tab Fig. 1. Open in new tabDownload slide Age-stage-specific survival rate (sxj) of Agasicles hygrophila reared on Alternantheraphiloxeroides grown under three different CO2 concentrations. Fig. 1. Open in new tabDownload slide Age-stage-specific survival rate (sxj) of Agasicles hygrophila reared on Alternantheraphiloxeroides grown under three different CO2 concentrations. Fig. 2. Open in new tabDownload slide Age-specific-survival rate (lx), fecundity (mx), and net maternity (lxmx) of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations. Fig. 2. Open in new tabDownload slide Age-specific-survival rate (lx), fecundity (mx), and net maternity (lxmx) of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations. Fig. 3. Open in new tabDownload slide Age-stage-specific survival expectancy (exj) of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations. Fig. 3. Open in new tabDownload slide Age-stage-specific survival expectancy (exj) of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations. Fig. 4. Open in new tabDownload slide Age-stage-specific reproductive value (vxj) of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations. Fig. 4. Open in new tabDownload slide Age-stage-specific reproductive value (vxj) of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations. Population Parameters of Ag. hygrophila The net reproductive rate (R0), intrinsic rate of increase (r), and finite rate of increase (λ) of Ag. hygrophila, reared on Al. philoxeroides grown under different CO2 concentrations showed significant differences and increased significantly with increasing CO2 concentrations. However, the mean generation times (T) and Nfr/Nf (the number of reproductive females/total females) showed no significant differences among the three treatments. The preadult survival rate in the 750 ppm CO2 treatment was 69.9% and substantially higher than in the other two treatments (49.2 and 51.0% at 420 and 550 ppm, respectively) (Table 2). The highest female and male proportions in cohorts were observed in the 750 ppm CO2 treatment. Ag. hygrophila Population Projection We plotted the simulated population growths of Ag. hygrophila reared on Al. philoxeroides grown under the three CO2 concentrations based on the calculated life tables (Fig. 5). Beginning with 10 newly laid eggs, Ag. hygrophila is capable of producing up to four generations within 100 d. In the 420, 550, and 750 ppm CO2 treatments, the final population sizes were 3,692, 431,382, and 8,190,155 individuals, respectively. The population size of Ag. hygrophila reared on Al. philoxeroides grown under 750 ppm CO2 was significantly larger than it was in either of the other two treatments. The growth rates (rj,t) of all stages fluctuated greatly (Fig. 6). Fig. 5. Open in new tabDownload slide Population growth of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations. Fig. 5. Open in new tabDownload slide Population growth of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations. Fig. 6. Open in new tabDownload slide Fluctuation of growth rate of each life stage of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations. The red dashed line is the intrinsic rate of increase. We set the scale range of y-axis from −0.4 to 0.4 to reveal the fluctuation of growth rate around the intrinsic rate. Fig. 6. Open in new tabDownload slide Fluctuation of growth rate of each life stage of Agasicles hygrophila reared on Alternanthera philoxeroides grown under three different CO2 concentrations. The red dashed line is the intrinsic rate of increase. We set the scale range of y-axis from −0.4 to 0.4 to reveal the fluctuation of growth rate around the intrinsic rate. Discussion In this study, the initial numbers of eggs used in the life table studies for the three CO2 treatments were 272, 287, and 292, respectively, of which 179, 204, and 239 subsequently hatched (Table 1), with respective hatch rates of 65.8, 71.0, and 81.8%. Because the eggs used for the different CO2 treatments were randomly selected from our laboratory colony reared at ambient CO2, they could not have been influenced by exposure to different CO2 concentrations, indicating that the higher hatch rate noted in the 750 ppm group was by chance. Jha et al. (2012) and Mou et al. (2015) presented convincing arguments for using only hatched (=viable) eggs to accurately estimate the population parameters. Following their advice, we used only hatched eggs when analyzing the life table raw data and calculating the survival rate and daily fecundity. Numerous studies have demonstrated the variable effects of elevated CO2 concentrations on the development, survival, and fecundity of insect populations. The developmental time and total lifespan of different insect species fed on host plants in elevated CO2 environments were found to be prolonged (Wu et al. 2007, Murray et al. 2013, Rao et al. 2014, Wang et al. 2014). In our studies, the developmental durations of the pre-adult stages of Ag. hygrophila (a mandibulate insect) were not significantly affected when they fed on Al. philoxeroides plants that had been grown in elevated CO2 environment (Table 1). Fu et al. (2016) noted that when Ag. hygrophila individuals were reared directly under conditions of elevated CO2 concentrations, the developmental durations of the egg, first instar larval and pupal stages, and adult longevity were all reduced. Our findings, therefore, indicate that there may be differences in the indirect versus direct effects of increasing CO2 concentration on Ag. hygrophila. Higher fecundity under elevated CO2 conditions has been demonstrated by Chen et al. (2005) for Aphis gossypii Glover (Hemiptera: Aphididae), and by Shi et al. (2014) for Nilaparvata lugens Stål (Hemiptera: Delphacidae). In this study, we found that the preadult survival rate and fecundity of Ag. hygrophila were significantly higher in those beetles reared on Al. philoxeroides grown under a CO2 concentration of 750 ppm than in beetles fed on plants grown under CO2 concentrations of 420 and 550 ppm. For comparison purposes, the Weibull function has often been used to fit age-specific survival curves (lx). However, Tuan et al. (2017) discussed some of the problems with applying the Weibull function. We compared the first ages when survival rates were <50 and <5% in different treatments based on the results of 100,000 bootstraps. This new methodology can be used to compare survival curves at any critical age. In the present study, the lengths of the APOPs and TPOPs associated with the elevated CO2 level were distinctly lower than those in the other two treatments, although the fecundity was higher. Based on these results, i.e., the shorter APOPs and TPOPs, the higher fecundities (F and Fr), the greater number of oviposition days (Od), and the number of eggs laid per oviposition day (Ed), Al. philoxeroides plants grown under an elevated CO2 environment (550 and 750 ppm) may have enhanced nutritive value which would be capable of stimulating the development of Ag. hygrophila’s reproductive system leading to earlier copulation, oviposition, and other reproductive behaviors. Given that the Od value provides a realistic measure of the number of days that females actually produced eggs, it is a better statistic than the commonly used parameter ‘oviposition period’, which does not delineate the number of days the females actually lay eggs. Furthermore, because Ed indicates the number of eggs laid per day during Od, it is, likewise, a better measure than the ‘eggs per day’ value derived from the entire oviposition period. Because Fr excludes females that are nonreproductive, it more accurately represents the actual fecundity of the reproductive females. We found that the R0,r, and λ values distinctly increased with increasing CO2 concentration, and that the mean generation time (T) was shorter. Because elevated CO2 levels were beneficial in terms of both female oviposition and survival, and increased male longevity, the higher fitness of Ag. hygrophila at elevated CO2 concentrations was clearly demonstrated by these population parameters. The detailed physiological mechanisms underlying these characteristics merit further research. If all biotic and abiotic conditions remain constant, the growth rate of all stages will theoretically approach the intrinsic rates of increase (r), i.e., 0.0715, 0.1180, and 0.1476/day in the 420, 550, and 750 ppm CO2 treatments, respectively, as time approaches infinity and the population settles down to the stable age-stage distribution (Huang and Chi 2012). In Figs. 5 and 6, we demonstrated the advantage of population projection based on the age-stage, two-sex life table over the traditional female age-specific life table in revealing the stage structure and fluctuation of growth rate of different stages. Moreover, our projections show that it would be inappropriate to use a single parameter, e.g., the intrinsic rate of increase or net reproductive rate, to predict the population growth before it settles down to the stable age-stage distribution. Although biological control is often an effective means of managing invasive plants, the probable variability in the responses of plant–insect interactions to climate change make it difficult to predict the future effectiveness of biological control programs (Reeves et al. 2015). Life tables can provide a comprehensive description of the fitness of an insect population on a given host plant (Reddy et al. 2015). In this regard, population growth can be projected using age-stage two-sex life tables, which potentially offer abundant information that can be utilized for effective biological control and other management strategies (Akköprü-Polat et al. 2015). Unlike traditional age-specific life tables, which deal only with female populations, neglect variations in the development rate among individuals, and cannot reveal stage differentiation (Lotka 1907, Birch 1948, Chi 1988, Carey 1993), the age-stage, two-sex life table theory developed by Chi and Liu (1985) incorporates both sexes and accounts for individual variations in developmental rate. Stage differentiation is critical to understanding population ecology in order to schedule pest management against a specific stage of an insect; especially since, significant stage overlapping phenomena have frequently been observed in many insect and mite species (Chi and Liu 1985). Age-stage, two-sex life tables have, therefore, been increasingly utilized in many studies in recent years (Yu et al. 2013, Fu et al. 2016, Liu et al. 2017), and should be considered more often in assessing the effectiveness of biological control programs. The present study demonstrated that elevated CO2 levels resulted in causing significant effects on the majority of the population parameters of Ag. hygrophila, i.e., the preadult survival, fecundity, Od, Ed, APOP, TPOP, R0,r, and λ. Elevated CO2 levels, consequently, benefited the reproduction of the beetles indirectly and favorably affected the control of Al. philoxeroides. The increased control efficacy was also demonstrated by using population projection. Future studies should examine the simultaneous effects of elevated CO2 on both Ag. hygrophila and Al. philoxeroides. Although we are currently undertaking research on this topic, the present study and newly initiated projects have been strictly laboratory based. Additional studies under more relevant field conditions will also be necessary. The first three authors, Meng-Zhu Shi, Jian-Yu Li and Bo Ding, contributed equally to this article. Acknowledgments We thank Dr. Cecil L. Smith (University of Georgia, USA) for language editing of this manuscript. The authors sincerely thank the many companies and students who provided assistance during the study, particularly in the culture of Al. philoxeroides and the collection of data. We are grateful to the anonymous reviewers and the editor for their valuable comments and suggestions, all of which greatly helped us in improving this article. 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TI - Indirect Effect of Elevated CO2 on Population Parameters and Growth of Agasicles hygrophila (Coleoptera: Chrysomelidae), a Biocontrol Agent of Alligatorweed (Amaranthaceae)
JF - Journal of Economic Entomology
DO - 10.1093/jee/toz015
DA - 2019-05-22
UR - https://www.deepdyve.com/lp/oxford-university-press/indirect-effect-of-elevated-co2-on-population-parameters-and-growth-of-0rEdRMwmQK
SP - 1120
VL - 112
IS - 3
DP - DeepDyve
ER -