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Influence of maize kernel state and type on life history of Plodia interpunctella (Lepidoptera: Pyralidae)
Journal of Stored Products Research 72 (2017) 121e127
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Influence of maize kernel state and type on life history of Plodia interpunctella (Lepidoptera: Pyralidae) Dragana Z. Predojevi c, M.Sc Teaching Assistant a, *, Filip N. Vukajlovi c a, zana B. Pesi ca Sne zana T. Tanaskovi c b, Sonja M. Gvozdenac c, Sne Faculty of Science, University of Kragujevac, Radoja Domanovica 12, 34000 Kragujevac, Serbia cak, Serbia Faculty of Agronomy, University of Kragujevac, Cara Dusana 34, 32000 Ca c Institute of Field and Vegetable Crops, Maksima Gorkog 30, 21000 Novi Sad, Serbia a
b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 21 April 2017 Accepted 21 April 2017
The objective of this study was to investigate the influence of different mechanical states (whole, broken and ground kernels) and types (dent, semi-flint and flint) of maize kernels on life history parameters of Plodia interpunctella (Hübner), the Indian meal moth. These parameters included larval development and its dynamics, adult emergence, mean development duration (MDD) and fecundity. Since the larvae are the developmental stage that causes the most damage on maize, additional data on larval development helps identify conditions that promote development. The results of our study indicate that broken maize kernels are the most suitable for P. interpunctella development, where the most successful larval development, the highest number of emerged adults, the shortest MDD and the highest total fecundity were recorded. On the contrary, whole kernels were the least suitable and the most resistant to infestation by P. interpunctella. The type of kernel also significantly affects P. interpunctella developmental parameters. Females reared on flint kernels (the hardest kernel type tested in our study) laid the largest total number of eggs, which implies that kernel hardness, i.e. the type of kernel should be an important parameter when choosing maize hybrids for cultivation and for storage. Our study warrants further investigation of maize types and their susceptibility to P. interpunctella. © 2017 Elsevier Ltd. All rights reserved.
Keywords: P. interpunctella Larval development Development duration Fecundity Corn
1. Introduction Plodia interpunctella (Hübner), the Indian meal moth, is a widespread lepidopteran storage pest (Mohandass et al., 2007). Due to the huge economical losses it causes to a wide range of stored food commodities (Sedlacek et al., 1995), P. interpunctella is possibly the most important insect pest in the world (Han et al., 2016). Larvae feed on raw and processed cereals and cereal products (Mbata, 1990; Stejskal et al., 2014), dried fruits and vegetables (Hamlin et al., 1931; Na and Ryoo, 2000; Perez-Mendoza and ~ a, 2004), pistachios (Razazzian et al., 2015), nuts Aguilera-Pen (Johnson et al., 1992) and confectionery products (Na and Ryoo, 2000). It is also found in flour and flour product storages, and mills (Doud and Phillips, 2000). The list of foods infested by this pest includes dried roots, spices and nut candies (Shepard, 1940).
* Corresponding author. Institute of Biology and Ecology, Faculty of Science, University of Kragujevac, Radoja Domanovi ca 12, 34000 Kragujevac, Serbia. E-mail address: [email protected] (D.Z. Predojevi c). http://dx.doi.org/10.1016/j.jspr.2017.04.010 0022-474X/© 2017 Elsevier Ltd. All rights reserved.
Plodia interpunctella larvae could be found in large numbers in stored maize (Arbogast, 2007; Kaliyan et al., 2005; Mbata, 1990; Stejskal et al., 2014; Throne and Arbogast, 2010). The survival of P. interpunctella in stored maize mostly depends on its larval survival, since larvae is the only feeding stage of this pest (Kaliyan et al., 2005). Larvae feed mostly on the germinal part of the maize kernel rather than on the endosperm, causing losses in seed viability (Abdel-Rahman et al., 1968), poor seed germination (Sallam, 1999) and deterioration of maize quality by contaminating it with webbing and feces (Phillips et al., 2000). Maize is the most important exporting crop in Serbia (Anonymous 1, 2016). However, no maize hybrids or kernel types in our country have been screened for susceptibility to P. interpunctella. The results of numerous studies indicate that the mechanical state of stored maize kernel influences P. interpunctella development and that the broken kernels are the most suitable for its development and survival (Kaliyan et al., 2005; Mbata, 1990). However, in most of these studies, detailed data about developmental dynamics on different mechanical states of maize kernels
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were not given. Generally, there has been little investigation of P. interpunctella larval developmental dynamics, therefore our research was done to gather additional data on suitability of ground maize to development of P. interpunctella. Based on the endosperm and kernel composition, there exist six maize kernel types (Anonymous 2, 2008). Flint, dent and some of its semi-types are the most commonly grown kernel types in Europe and North America. The basic difference among these types of kernel is in the proportion of floury and horny endosperm, which differs among them (Anonymous 2, 2008). Flint kernels have high percentage of horny endosperm around the small soft center, while dent kernels have horny endosperm on the sides and the base of the kernel (Anonymous 2, 2008). According to the CIMMYT/IBPGR (1991) description, semi-flint maize kernels are flint kernels with a soft cup. Floury endosperm is softer and easier to break than horny endosperm (Babic et al., 2013). The type and ratio of endosperm in maize are directly connected to kernel hardness (Vieira Filho et al., 2015). Very few maize hybrids and kernel types have been tested for susceptibility to any storage insect pests. Harris and Green (1959) reported that damage caused by Sitophilus oryzae (L. 1763), was low on flint kernels, medium on semi flint kernels and the highest on dent varieties of maize. Our hypothesis was that kernel hardness significantly influences the life history of P. interpunctella, i.e., harder maize kernels would be less vulnerable to damage caused by P. interpunctella. Testing kernel hardness and continuous improving of kernel resistance to the attacks of storage insect pests could provide smaller losses in the quality and quantity of stored cereals in the future. Kernel hardness should be an important parameter when choosing maize hybrid for growing. It has been known that fecundity, development time and other biological parameters of P. interpunctella depend on the food source (Mohandass et al., 2007). The objective of our research was to investigate the influence of different mechanical states (whole, broken and ground kernels) and types (dent, semi flint and flint) of maize kernels to P. interpunctella life history. We wanted to determine whether P. interpunctella life history parameters (larval development and its dynamics, adult emergence, mean development duration and fecundity) depend on maize kernel state and type. Synergistic effects regarding type and state of kernels on P. interpunctella development history were also investigated. 2. Materials and methods 2.1. Maize kernels The experiment was carried out by using the following maize hybrids as nutrient mediums: NS 6130 (FAO 600), an experimental NS hybrid (FAO 600) and NS 1090 (FAO 170e190). All of the tested maize hybrids were in different type of kernel - dent, flint and semi-flint, respectively. Three mechanical states of kernels were used: whole undamaged kernels, mechanically broken kernels and ground kernels (whole grain corn flour). Maize hybrids were selections obtained from the Institute of Field and Vegetable Crops, Novi Sad, Republic of Serbia. The kernels were not treated with insecticides after the harvest or before setting up the experiment. Before starting the experiment, all of the used kernels were exposed to deep freezing (80 C), in order to eliminate possible presence of storage insect pests and parasites. 2.2. Insect cultures Plodia interpunctella cultures used in this research originated from a population reared for several years in The Laboratory for General and Applied Entomology, Faculty of Science, University of
Kragujevac, Serbia. Parental populations were reared in transparent plastic containers for mass rearing (1.2 L in volume), at chamber set at 28 ± 1 C, r.h. 60 ± 10% and 14:10 (L:D) photoperiod, on a standard laboratory diet for P. interpunctella (Silhacek and Miller, 1972). Moths in copuli were isolated from mass rearing containers and placed into oviposition jars, to collect one-day-old P. interpunctella eggs. Before the actual experiment, eggs were observed with a binocular microscope to eliminate those with obvious deformities. 2.3. Experimental design The experiment was set up as a randomized 3 3 4 block design type. We used three types of maize kernels (dent, semi flint and flint), in three different mechanical states. Each kernel type and state was repeated four times, with a total of 36 assays. The experiment was carried out by placing 100 g of mentioned kernel type and state into 0.25 L glass jars, in which 100 one-day-old P. interpunctella eggs were added. Jars were sealed with swab of cotton, coated with cotton cloth, for proper aeration. The experiment was carried out in environmental conditions described for the rearing of parental moth population. 2.4. Experimental procedure Ten days after setting up the experiment, larvae were collected from the hatched eggs. The examination started ten days after the beginning of the experiment, because 5e7 days old larvae were not easily noticeable, due to their very small size, light color and preference to hide inside the kernel. The head capsule width was measured for all collected larvae, using an ocular micrometer of binocular microscope. Based on the data obtained, different larval instars were distinguished (Allotey and Goswami, 1990) and the duration and dynamics of larval development period was determined. After the first examination, these actions were repeated every five days, until the last larva became a pupa. Once the emergence of the adults began, assays were checked once every 12 h and the number of the emerged adults and their gender was recorded. After that, newly emerged unmated adults from the same assay were immediately paired and each pair in copuli was isolated in a separate test tube. In order to obtain fecundity data, the number of eggs laid per female was recorded daily until the females died. The fecundity was defined as the total number of eggs laid after the mating. In the end of the experiment, the mean development duration (MDD) was calculated for each P. interpunctella adult, as the average time (in days), from the start of the experiment to each adult emergence. Based on the percentage of adult emergence and the mean values of MDD, the susceptibility index (Dobie, 1974) was calculated, according to the Howe's method (1971). 2.5. Statistical analysis Data were statistically analyzed using the IBM SPSS Statistics 21 software package (IBM, 2012). A two-way analysis of variance (ANOVA) was carried out to test the influence of the state and the type of kernels, as well as their synergistic effect on the larval development of P. interpunctella. Means of head capsule width among different state and type of kernel were compared using the multiple comparisons Tukey HSD test (P < 0.05). A one-way ANOVA was performed to test the influence of kernel state and type on the MDD and fecundity. Means of MDD and fecundity among different state and type of kernel were compared using the Dunnet T3 test (P < 0.05).
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3. Results 3.1. Larval development The results on duration and dynamics of larval development tested on three maize kernel states and types are presented in Tables 1e3. The fastest development and the highest increase in head capsule width were recorded between the 10th and 15th day of larval development, on all states and types of maize kernels. In this period, larvae doubled the width of their head capsule. Larvae reared on broken kernels reached the fifth instar five days earlier than on ground kernels and ten days earlier than those reared on whole kernels. Larval development was the shortest on ground kernels and it lasted for 30 days on all three kernel types. However, the number of individuals that finished the life cycle was the highest on broken kernels, although their larval development lasted for 35e40 days. The duration and dynamics of larval development differed among three tested maize kernel states and types (Table 4). The mechanical state and type of kernels as well as the synergistic effect between these two factors had influenced the larval development (Table 4). The mechanical state of kernels had the most significant influence. State of kernels had significant influence during almost the entire period of larval development, except in the period between 10th and 15th day (Table 4). Type of kernels, had statistically significant influence, although lower than the state of kernels, even during the 10th to 15th day period, up until 25th day of larval development (Table 4). The synergistic effect of state and type of kernel on P. interpunctella larval development also existed, especially during the first 15 days (Table 4).
3.2. Adult emergence and mean developmental duration The results on the mean number of emerged adults and mean developmental duration (MDD) are presented in Table 5. The highest mean number of emerged adults was recorded on broken kernels, while the lowest on whole ones. There were no statistically significant differences in the number of emerged adults among different kernel types in the state of broken and ground kernels (F2,9 ¼ 0.698, P ¼ 0.523; F2,9 ¼ 0.707, P ¼ 0.519, respectively). However, there were some statistically significant differences in number of emerged adults on whole kernels, but only between dent and semi-flint type (P ¼ 0.027). State of kernel showed high influence on the number of emerged adults. Significant differences
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were recorded between number of emerged adults on whole and broken (P < 0.0005), as well as between whole and ground kernels (P < 0.0005). The shortest MDD have had moths in assays with broken dent kernels (34 d), while the longest MDD have had those reared on ground semi-flint kernels (47 d). The state of kernels showed statistically significant influence on P. interpunctella MDD, unlike the type of kernels (Table 5). Moths reared on broken dent kernels had significantly shorter MDD (34 d), compared to those reared on whole and ground dent kernels (38.5 d; 46 d; P ¼ 0.042; P < 0.0005, respectively). Similar and significant effects of kernel state on MDD were observed for semi-flint kernels. Moths reared on whole and broken semi-flint kernels had significantly shorter MDD (37.2 d, 38 d, respectively), compared to those reared on ground semi-flint kernels (47 d; P ¼ 0.003; P ¼ 0.001, respectively). There were no significant differences in MDD among different states of flint kernel type (F2,11 ¼ 3.521; P ¼ 0.074). 3.3. Susceptibility indices of different maize kernel state and type to infestation by P. interpunctella Susceptibility indices for the development of P. interpunctella on different types and states of maize kernels are given in Table 5. According to Mensah (1986), maize hybrids with susceptibility indices less than 2.5 are considered to be resistant to infestation by P. interpunctella. In our study, this includes whole kernels in the type of dent and flint, but not the semi-flint, which was medium resistant. The medium resistant kernels were those with values of susceptibility indices between 2.6 and 5. The kernels with susceptibility indices between 7.6 and 10.00 were deemed as susceptible to infestation by P. interpunctella. All types of broken kernels belong to this group (Table 5). Based on results of Dobbie index of susceptibility, all types of ground kernels were considered as moderately susceptible to infestation by P. interpunctella, with indices values between 5.1 and 7.5. The highest values of susceptibility index were for broken flint kernels (9.72), while the lowest were for whole dent kernels (1.81). Suitability of maize kernel is not influenced by the type of kernel, but only with the state of kernel (P < 0.0005) (Table 5). 3.4. Fecundity Results on the total number of mated adults and average fecundity are shown in Table 6. On average, fecundity was the
Table 1 Mean (±SE) larval head capsule widths (in mm), larval instars, comparison among instars and mean growth ratio of Plodia interpunctella reared on whole, broken and ground dent kernels. State of kernel
Number of days since the beginning of the experiment 10
15
20
25
30
35
40
H. w. (mm)a (±SE) Instar C. I. Ratio
0.193 (±0.006) I e
H. w. (mm)a (±SE) Instar C. I. Ratio
0.306 (±0.009) I e
Ground
H. w. (mm)a (±SE) Instar C. I. Ratio
0.21 (±0.007) I e
0.656 (±0.033) III III/II 1.7 0.908 (±0.009) V V20 d/II 1.63 0.59 (±0.011) III III-II 1.44
0.861 (±0.221) V V25 d/III 1.31 1.127 (±0.015) V V25 d/V20 d 1.24 0.91 (±0.006) V V25 d/III 1.54
1.081 (±0.048) V V30 d/V25 d 1.25 1.246 (±0.03) V V30 d/V25 d 1.105 1.04 (±0.022) V V30 d/V25 d 1.14
1.137 (±0.087) V V35 d/V30 d 1.05 1.252 (±0.06) V V35 d/V30 d 1.005 e
e
Broken
0.386 (±0.019) II II/I 2.0 0.555 (±0.01) II II-I 1.81 0.41 (±0.005) II II/I 1.95
e
e
Whole
e 1.3 (±0.06) V V40 d/V35 d 1.04 e
C. I. e Compared Instars. a H. W. (mm) e each datum is calculated based on the mean values of head capsule width (in mm) measured for all collected larvae in four replicates (for each state of dent kernel type).
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Table 2 Mean (±SE) larval head capsule widths (in mm), larval instars, comparison among instars and mean growth ratio of Plodia interpunctella reared on whole, broken and ground semi-flint kernels. State of kernel
Number of days since the beginning of the experiment 10
15
20
25
30
35
40
Whole
a
H. w. (mm) (±SE) Instar C. I. Ratio
0.143 (±0.018) I e
Broken
H. w. (mm)a (±SE) Instar C. I. Ratio
0.256 (±0.009) I e 0.23 (±0.008) I e
0.693 (±0.04) III III/II 1.925 0.972 (±0.015) V V20 d/III 1.5 0.66 (±0.09) III III/II 1.57
0.75 (±0.04) IV IV/III 1.08 1.056 (±0.023) V V25 d/V20 d 1.09 0.93 (±0.0007) V V25 d/III 1.4
1.09 (±0.198) V V30 d/IV 1.45 1.211 (±0.026) V V30 d/V25 d 1.15 1.05 (±0.012) V V30 d/V25 d 1.13
1.225 (±0.037) V V35 d/V30 d 0.97 1.325 (±0.03) V V35 d/V30 d 1.09 e
1.267 (±0.028) V V40 d/V35 d 1.03 1.4-V
H. w. (mm)a (±SE) Instar C. I. Ratio
0.36 (±0.031) II II/I 2.52 0.64 (±0.013) III III/I 2.5 0.42 (±0.005) II II/I 1.82
e
e
Ground
V40 d/V35 1.056 e
d
C. I. e Compared Instars. a H. W. (mm) e each datum is calculated based on the mean values of head capsule width (in mm) measured for all collected larvae in four replicates, for each state of semiflint kernel type.
Table 3 Mean (±SE) larval head capsule widths (in mm), larval instars, comparison among instars and mean growth ratio of Plodia interpunctella reared on whole, broken and ground flint kernels. State of kernel
Whole
Broken
Ground
Number of days since the beginning of the experiment 10
15
20
25
30
35
40
H. w. (mm)a (±SE) Instar C. I. Ratio
0.19 (±0.008) I e 0.321 (±0.009) I
0.75 (±0.036) IV IV/III 1.2 1.226 (±0.013) V
1.021 (±0.034) V V30 d/IV 1.36 1.248 (±0.03) V
1.105 (±0.062) V V35 d/V30 d 1.08 1.256 (±0.06) V
C. I. Ratio
e 0.23 (±0.008) I e
V25 d/V20 d 1.3 0.92 (±0.001) V V25 d/III 1.37
V30 d/V25 d 1.02 0.95 (±0.002) V V25 d/V20 d 1.03
V35 d/V30 1 e
e
H. w. (mm)a (±SE) Instar C. I. Ratio
0.626 (±0.03) III III/II 1.51 0.945 (±0.01) V V20 d/IV 1.26 0.67 (±0.009) III III/II 1.56
1.2-V
H. w. (mm)a (±SE) Instar
0.413 (±0.017) II II/I 2.17 0.747 (±0.014) IV IV-I 2.33 0.43 (±0.007) II II/I 1.87
d
e
V40 d/V35 1.08 e
d
e e
C. I. e Compared Instars. a H. W. (mm) e each datum is calculated based on the mean values of head capsule width (in mm) measured for all collected larvae in four replicates, for each state of flint kernel type.
Table 4 Statistical analysis of influence of different maize kernel states, types and their synergistic effect on differences in head capsule width of Plodia interpunctella larvae. Number of days since the beginning of the experiment
State of kernela
Type of kernela
Synergistic effectb
10
15
20
25
30
35
40
F ¼ 88.647 df ¼ 2,36 P < 0.0005* F ¼ 5.582 df ¼ 2,36 P ¼ 0.004* F ¼ 3.609 df ¼ 4,36 P ¼ 0.006*
F ¼ 0.979 df ¼ 2,36 P ¼ 0.376 F ¼ 6.270 df ¼ 2,36 P ¼ 0.002* F ¼ 22.889 df ¼ 4,36 P < 0.0005*
F ¼ 133.353 df ¼ 2,36 P < 0.0005* F ¼ 4.254 df ¼ 2,36 P ¼ 0.025* F ¼ 1.074 df ¼ 4,36 P ¼ 0.389
F ¼ 232.024 df ¼ 2,36 P < 0.0005* F ¼ 8.484 df ¼ 2,36 P ¼ 0.001* F ¼ 10.392 df ¼ 4,36 P < 0.0005*
F ¼ 9.910 df ¼ 2,36 P ¼ 0.001* F ¼ 0.802 df ¼ 2,36 P ¼ 0.459 F ¼ 0.906 df ¼ 4,36 P ¼ 0.475
F ¼ 12.885 df ¼ 2,36 P < 0.0005* F ¼ 0.043 df ¼ 2,36 P ¼ 0.958 F ¼ 1.522 df ¼ 4,36 P ¼ 0.224
F ¼ 3.846 df ¼ 2,36 P ¼ 0.034* F ¼ 1.871 df ¼ 2,36 P ¼ 0.173 F ¼ 3.957 df ¼ 4,36 P ¼ 0.012*
(a)Each datum is statistically analyzed based on the mean width of larval head capsule measured for all collected larvae in four and (b) eight replicates, each set up with 100 eggs. P values having asterisk (*) in superscript are significantly different by two-way ANOVA and Tukey HSD test at P < 0.05.
highest for moths reared on broken kernels, followed by those reared on ground and whole ones. The highest fecundity was recorded on broken dent, while the lowest on whole dent kernels. There were no statistically significant differences in fecundity among different kernel types in the state of whole and broken kernels (F2,7 ¼ 2.121, P ¼ 0.190; F2,127 ¼ 0.062, P ¼ 0.940,
respectively). However, there were some statistically significant differences in fecundity on ground kernels, among dent, semi-flint and flint type (P < 0.0005; P < 0.0005, P < 0.0005, respectively). When comparing fecundity among different states of one kernel type, there were some significant differences. Mean fecundity on broken and ground dent kernels were significantly higher than on
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Table 5 Mean number of emerged adults, mean developmental duration and mean susceptibility index (±SE) of Plodia interpunctella on different kernel states (whole, broken and ground) and types of maize. State of kernels
Maize kernel type
Mean number of emerged adults ± SE
Mean developmental duration ± SE
Mean susceptibility index ± SE
Whole
Dent Semi flint Flint Dent Semi flint Flint Dent Semi flint Flint
1.75 ± 0.25a1 4.25 ± 0.85b2 2.25 ± 0.25c 27.25 ± 3.84 28.25 ± 2.78 32 ± 2.12 18.75 ± 1.93 24.5 ± 5.33 18.5 ± 4.09
38.5 ± 0.64 a 37.2 ± 2.831 42.4 ± 3.53 34 ± 1.5 b 38 ± 2.061 35.7 ± 1.41 46 ± 0.82 c 47 ± 0.412 43.5 ± 0.64
1.81 3.69 1.94 9.67 8.87 9.72 6.34 6.68 6.54
Broken
Ground
± ± ± ± ± ± ± ± ±
0.041 (R)* 0.66 (MR) * 0.37 (R) * 0.447 (S) * 0.72 (S) * 0.34 (S) * 0.16 (MS) * 0.43 (MS) * 0.59 (MS) *
R e resistant; MR e medium resistant; S e susceptible; MS e medium susceptible (Mensah, 1986). Vertical mean values of number of emerged adults and MDD having different letter (a, b, c, for compared different states of kernel) or different number (1, 2, for compared different types of kernel) in superscript are statistically different by one-way ANOVA test and Dunnet T3 test at P < 0.05. Vertical values of mean susceptibility index among different state of one kernel type having asterisk (*) in superscript are statistically different by one-way ANOVA test and Bonferroni at P < 0.05.
Table 6 The total number of mated Plodia interpunctella females and their mean fecundity on different maize kernel states and types. Maize kernel type
Whole kernels Mated females
Dent Semi flint Flint Mean fecundity
4 4 2
Broken kernels Fecundity
Mated females
Range
Mean ± SE
22e44 33e154 40e95
27.75 ± 5.42b 81 ± 25.73a,b 67.5 ± 27.5a,b 57 ± 13.23
38 35 57
Ground kernels Fecundity
Mated females
Range
Mean ± SE
18e225 19e171 16e178
113.37 109.94 109.42 110.42
± ± ± ±
7.99a 7.04a 4.57a 3.58
12 23 17
Fecundity Range
Mean ± SE
96e170 43e92 65e95
114.33 ± 6.17a* 61.17 ± 2.33b* 79.76 ± 1.74b* 79.52 ± 3.41
Horizontal values having different letter (a, b, c) in superscript are statistically different by one-way ANOVA test and Dunnet T3 test at P < 0.05. Vertical values having asterisk (*) in superscript are statistically different by one-way ANOVA and Dunnet T3 test at P < 0.05.
whole ones (P < 0.0005, P < 0.0005, respectively). Highly significant differences were recorded between broken and ground kernels for both semi-flint and flint (P < 0.0005, P < 0.0005, respectively). There were no significant differences when comparing fecundity on broken and ground kernels to fecundity on whole kernels for semiflint (P ¼ 0.656; P ¼ 0.828, respectively) and flint (P ¼ 0.989; P ¼ 0.923, respectively) (Table 6). 4. Discussion Several studies have been conducted to determine the effect of maize variety on the development and survival of P. interpunctella, to identify different resistant varieties (Abdel-Rahman et al., 1968; Mbata, 1990). Results of our study have shown that mechanical state and type of kernels, as well as their synergistic effect, highly influences larval development, based on head capsule width measurements and survival of P. interpunctella adults. The mechanical state of kernels had a higher influence on larval development and number of emerged adults, succeeded by the type of kernels and synergy effect of kernel state and type. The data on the development time of individual instars of P. interpunctella is limited in the published literature (Mohandass et al., 2007). Results of our study have shown that feeding on broken kernels has led to the fastest development, the highest increase in head capsule width and the highest rate of survival of adults. This is in accordance with results of Mbata (1990) who reported that, when reared on broken maize kernels, P. interpunctella larvae usually developed significantly faster, compared to the development speed of those reared on whole maize kernels. LeCato (1976) found that cracked and ground kernels were more favorable for growth, development and production of P. interpunctella adult progeny. According to Kaliyan et al. (2005), a very low percentage
of larvae survived on whole kernels (7e28%). The results of our study are in accordance with these literature published data. Mbata (1990) and Kaliyan et al. (2005) suggested that the integrity of maize kernels is crucial for protection of stored maize, since whole kernels are much less susceptible to attack by P. interpunctella larvae. The results of our study confirm that whole kernels are the most resistant to infestation by P. interpunctella, unlike ground and broken ones which are medium susceptible or susceptible to infestation, respectively. The longest MDD was perceived with moths reared on ground kernels. This prolonged development has led to smaller number of emerged moths than we had expected based on the number of larvae registered during the head capsule measurements. Other authors have already confirmed negative correlation between duration of larval development and the number of emerged adults. Williams (1964) reported that mortality of pre-adult stages is usually higher in prolonged developmental period. Means of MDD reported here are in accordance with literature data: 28.4e35.3 days (Abdel-Rahman et al., 1968) and 34.5 days (Arbogast, 2007) on whole maize kernels; 25.9e38 days (Mbata, 1990) and 28.5 days (Imura and Sinha, 1986) on broken kernels; 28.05 days in ground maize (Allotey and Goswami, 1990). Fecundity was also significantly influenced by mechanical state of kernels since the highest fecundity was on broken and the lowest on whole kernels. Only a few studies reported values of fecundity of P. interpunctella reared on maize. Fecundity of moth population from farm-stored maize was 208.1 (Arbogast, 2007), while 174.2 on broken maize kernels (Allotey and Goswami, 1990). Lower values of average fecundity reported in our study could be explained by Nansen and Phillips (2003) findings. These authors showed that, when mated, females were prevented from directly coming into contact with the food
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source, oviposition was significantly reduced. Mbata (1990) also reported that the number of eggs laid on maize varieties was significantly higher than the number deposited on the glass (empty Petri dish). In our experiment, females were isolated and laid eggs in empty glass test tubes. Larval survival and fecundity were influenced by the type of kernels, especially by broken and ground ones. Influence of different types of kernel is mainly based on differences in kernel structure and hardness. This is confirmed by Abdel-Rahman et al. (1968) who also suggest that numerical differences in larval survival among different maize varieties may be due to difference in kernel hardness. The influence of type of kernel on life history parameters of P. interpunctella was especially obvious when comparing fecundity among different types of broken and ground kernels. Females reared on dent kernel type laid the largest mean number of eggs, both on broken and ground kernels, with statistical differences only on different types of ground kernels. Dent kernel type was the softest kernel type tested in our study. It contains higher percentage of floury endosperm, which is softer and easier to break (Babic et al., 2013). Easier consumption of dent kernels and lower energy cost for breaking the kernel pericarp, might lead to higher mean fecundity. However, the highest total number of mated females and number of laid eggs were recorded on broken flint kernels, the hardest kernel type tested in our study. This can be due to highest percentage of horny endosperm, which have higher proportion of protein matrix (Babi c et al., 2013). It is well known that population size and developmental dynamics of P. interpunctella depends on both nutritive quality and mechanical state of available food (Locatelli and Limonta, 1998). Data on mean fecundity of P. interpunctella reared on different types of broken and ground kernels are limited in the published literature. The only available data about dependence of P. interpunctella fecundity on whole maize kernels of different type were given by Abdel-Rahman et al. (1968). These authors found that differences in fecundity of moths reared on whole kernels of different maize varieties were not significant, which is in accordance with our results. Synergistic effects of kernel state and type showed statistically significant influence during the first 15 days of larval development. During the mentioned period, while examining jars in search for larvae to measure, we noticed that larvae primarily attack the part of the kernel where the germ is, while the pericarp was the least damaged. This confirms that pericarp presents a barrier to larval attacks, which was also reported by Abdel-Rahman et al. (1968), LeCato (1976) and Sallam (1999). Although the mandibles of larvae are strong, they have difficulties in breaking the greatly resistant maize pericarp (Locatelli and Limonta, 1998; Kaliyan et al., 2005). This is the reason why larval development was mostly influenced by state of kernels from the 20th day and why only 33 adults (out of 1200 eggs added at the beginning of the experiment) emerged on whole kernels. In recent studies, Limonta et al. (2013) tested susceptibility of different maize variants to P. interpunctella and showed that larval penetration into the kernel was influenced by maize embryo properties; mutant seeds lacking embryos were less damaged and therefore showed the lowest mean number of adult insects. Acknowledgements This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. We are thankful to Zeljko Milovac, PhD, for supplying us with maize kernels from Institute of Field and Vegetable Crops, Novi Sad, Serbia.
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A wild strain of Plodia interpunctella (Hübner) from farm-stored maize in South Carolina. Effect of temperature on mating, survival, and fecundity. J. Stored Prod. Res. 43, 503e507. Babi c, L.J., Radoj cin, M., Pavkov, I., Babi c, M., Turan, J., Zoranovi c, M., Stanisi c, S., 2013. Physical properties and compression loading behavior of corn seed. Int. Agrophy. 27, 19e126. Dobie, P.,1974. The laboratory assessment of the inherent susceptibility of maize varieties to post-harvest infestation by Sitophilus zeamais. J. Stored Prod. Res. 10, 183e197. Doud, C.W., Phillips, T.W., 2000. Activity of Plodia interpunctella (Lepidoptera: Pyralidae) in and around flour mills. J. Econ. Entomol. 93 (6), 1842e1847. Hamlin, J.C., Reed, W.D., Phillips, M.E., 1931. Biology of the Indianmeal moth on dried fruits in California. USDA Tech. Bull. 242, 27. Han, G.D., Kwon, H., Na, J., Kim, Y.H., Kim, W., 2016. Sensitivity of different life stages of Indian meal moth Plodia interpunctella to gaseous chlorine dioxide. J. Stored Prod. Res. 69, 217e220. Harris, E.D., Green, V.E., 1959. Comparison of Field corn varieties for resistance to corn earworm and stored grain insect injury in the everglades. Fla. Entomol. 42, 11e16. Howe, R.W., 1971. A parameter for expressing the suitability of environment for insect development. J. Stored Prod. Res. 7, 63e65. IBM Corp Released, 2012. IBM SPSS Statistics for Windows. Version 21.0. IBM Corp, Armonk, NY. IBPGR, 1991. Descriptors for Maize. International Maize and Wheat Improvement Center. Mexico City/International Board for Plant Genetic Resources, Rome. ISBN 92-9043-189-1. Imura, O., Sinha, R.N., 1986. Bioenergetics of the Indianmeal moth, Plodia interpunctella (Lepidoptera: Pyralidae). Ann. Entomol. Soc. Am. 73, 96e103. Johnson, J.A., Wofford, P.L., Whitehand, L.C., 1992. Effect of diet and temperature on development rates, survival and reproduction of the Indianmeal moth (Lepidoptera: Pyralidae). J. Econ. Entomol. 85 (2), 561e566. Kaliyan, N., Carrillo, M.A., Morey, V., Wilcke, W.F., Cannon, C.A., 2005. Indian meal moth survivability in stored corn with different levels of broken kernels. Gt. Lakes. Entomol. 38 (3 & 4), 177e185. LeCato, G.L., 1976. Yield, development, and weight of Cadra cautella (Walker) and Plodia interpunctella (Hübner) on twenty-one diets derived from natural products. J. Stored Prod. Res. 12, 43e47. Limonta, L., Locatelli, D.P., Sangiorgio, S., Consonni, G., 2013. Susceptibility of maize variants to Plodia interpunctella. Ital. J. Food Sci. 25 (3), 283e288. Locatelli, D.P., Limonta, L., 1998. Development of Ephestia kuehniella (Zeller), Plodia interpunctella (Hübner) and Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae) on kernels and wholemeal flours of Fagopyrum esculentum (Moench) and Triticum aestivum L. J. Stored Prod. Res. 34 (4), 269e276. Mbata, G.N., 1990. Suitability of maize varieties for the oviposition and development of Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae). Trop. Pest Manag. 36 (2), 122e127. Mensah, G.W.K., 1986. Infestation potential of Callosobruchus maculates (F) (Coleoptera: Bruchidae) on cowpea stored under subtropical conditions. Int. J. Trop. Insect Sci. 7 (6), 718e784. Mohandass, S., Arthur, F.H., Zhu, K.Y., Throne, J.E., 2007. Biology and management of Plodia interpunctella (Lepidoptera: Pyralidae) in stored products. J. Stored Prod. Res. 43, 302e311. Na, J.H., Ryoo, I.M., 2000. The influence of temperature on development of Plodia interpunctella (Lepidoptera: Pyralidae) on dried vegetable commodities. J. Stored Prod. Res. 36, 125e129. Nansen, C., Phillips, T.W., 2003. Ovipositional responses of the Indianmeal moth, Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae) to oils. Ann. Entomol. Soc. Am. 96 (4), 524e531. ~ a, М., 2004. Development, reproduction, and conPerez-Mendoza, J., Aguilera-Pen trol of the Indian meal moth, Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae) in stored seed garlic in Mexico. J. Stored Prod. Res. 40, 409e421. Phillips, T.W., Berbert, R.C., Cuperus, G.W., 2000. Post-harvest integrated pest management. In: Francis, F.J. (Ed.), Encyclopedia of Food Science and Technology, second ed. Wiley Inc., New York, pp. 2690e2701. Razazzian, S., Hassani, M.R., Imani, S., Shojai, M., 2015. Life table parameters of Plodia interpunctella (Lepidoptera: Pyralidae) on four commercial pistachio cultivars. J. Asia-Pacific Entomol. 18, 55e59. Sallam, N.M., 1999. Danilo Mejia. In: ISIPE, F.A.O. (Ed.), Insect Damage: Damage on Post-harvest, p. 18.
D.Z. Predojevic et al. / Journal of Stored Products Research 72 (2017) 121e127 Sedlacek, J.D., Weston, P.A., Barney, J., 1995. Lepidoptera and Psocoptera. In: Subramanyam, Bh, Hagstrum, D.W. (Eds.), Integrated Management of Insects in Stored Products. Marcel Dekker, Inc., New York, pp. 41e70. Shepard, H.H., 1940. Insects Infesting Stored Foods. Minnesota Agricultural Experiment Station (Retrieved from the University of Minnesota Digital Conservancy). Silhacek, D.L., Miller, G.L., 1972. Growth and development of the Indian meal moth Plodia interpunctella (Lepidoptera: Phycitidae) under laboratory mass-rearing conditions. Ann. Entomol. Soc. Am. 65, 1084e1087. Stejskal, V., Aulický, R., Kucerova, Z., 2014. Pest control strategies and damage potential of seed-infesting Pests in the Czech Stores e a review. Plant Prot. Sci. 50,
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167e173. Throne, J.E., Arbogast, R.T., 2010. A computer model for simulating population development of the Indian meal moth (Lepidoptera: Pyralidae) in stored corn. J. Econ. Entomol. 103 (4), 1503e1507. Vieira Filho, J.A., Garcia, E.A., Seraphim, O.J., Floriano Murakami, E.S., de Britto ~o dos Santos, G., 2015. Maize kernel size and texture: Molino, A., Conceiça production parameters, quality of eggs of the laying hens and electricity intake. Acta Sci. 37, 29e33. Williams, G.C., 1964. The life-history of the Indian meal-moth, Plodia interpunctella (Hübner) (Lep. Phycitidae) in a warehouse in Britain and on different foods. Ann. Appl. Biol. 53, 459e475.
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Influence of maize kernel state and type on life history of Plodia interpunctella (Lepidoptera: Pyralidae) Dragana Z. Predojevi c, M.Sc Teaching Assistant a, *, Filip N. Vukajlovi c a, zana B. Pesi ca Sne zana T. Tanaskovi c b, Sonja M. Gvozdenac c, Sne Faculty of Science, University of Kragujevac, Radoja Domanovica 12, 34000 Kragujevac, Serbia cak, Serbia Faculty of Agronomy, University of Kragujevac, Cara Dusana 34, 32000 Ca c Institute of Field and Vegetable Crops, Maksima Gorkog 30, 21000 Novi Sad, Serbia a
b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 21 April 2017 Accepted 21 April 2017
The objective of this study was to investigate the influence of different mechanical states (whole, broken and ground kernels) and types (dent, semi-flint and flint) of maize kernels on life history parameters of Plodia interpunctella (Hübner), the Indian meal moth. These parameters included larval development and its dynamics, adult emergence, mean development duration (MDD) and fecundity. Since the larvae are the developmental stage that causes the most damage on maize, additional data on larval development helps identify conditions that promote development. The results of our study indicate that broken maize kernels are the most suitable for P. interpunctella development, where the most successful larval development, the highest number of emerged adults, the shortest MDD and the highest total fecundity were recorded. On the contrary, whole kernels were the least suitable and the most resistant to infestation by P. interpunctella. The type of kernel also significantly affects P. interpunctella developmental parameters. Females reared on flint kernels (the hardest kernel type tested in our study) laid the largest total number of eggs, which implies that kernel hardness, i.e. the type of kernel should be an important parameter when choosing maize hybrids for cultivation and for storage. Our study warrants further investigation of maize types and their susceptibility to P. interpunctella. © 2017 Elsevier Ltd. All rights reserved.
Keywords: P. interpunctella Larval development Development duration Fecundity Corn
1. Introduction Plodia interpunctella (Hübner), the Indian meal moth, is a widespread lepidopteran storage pest (Mohandass et al., 2007). Due to the huge economical losses it causes to a wide range of stored food commodities (Sedlacek et al., 1995), P. interpunctella is possibly the most important insect pest in the world (Han et al., 2016). Larvae feed on raw and processed cereals and cereal products (Mbata, 1990; Stejskal et al., 2014), dried fruits and vegetables (Hamlin et al., 1931; Na and Ryoo, 2000; Perez-Mendoza and ~ a, 2004), pistachios (Razazzian et al., 2015), nuts Aguilera-Pen (Johnson et al., 1992) and confectionery products (Na and Ryoo, 2000). It is also found in flour and flour product storages, and mills (Doud and Phillips, 2000). The list of foods infested by this pest includes dried roots, spices and nut candies (Shepard, 1940).
* Corresponding author. Institute of Biology and Ecology, Faculty of Science, University of Kragujevac, Radoja Domanovi ca 12, 34000 Kragujevac, Serbia. E-mail address: [email protected] (D.Z. Predojevi c). http://dx.doi.org/10.1016/j.jspr.2017.04.010 0022-474X/© 2017 Elsevier Ltd. All rights reserved.
Plodia interpunctella larvae could be found in large numbers in stored maize (Arbogast, 2007; Kaliyan et al., 2005; Mbata, 1990; Stejskal et al., 2014; Throne and Arbogast, 2010). The survival of P. interpunctella in stored maize mostly depends on its larval survival, since larvae is the only feeding stage of this pest (Kaliyan et al., 2005). Larvae feed mostly on the germinal part of the maize kernel rather than on the endosperm, causing losses in seed viability (Abdel-Rahman et al., 1968), poor seed germination (Sallam, 1999) and deterioration of maize quality by contaminating it with webbing and feces (Phillips et al., 2000). Maize is the most important exporting crop in Serbia (Anonymous 1, 2016). However, no maize hybrids or kernel types in our country have been screened for susceptibility to P. interpunctella. The results of numerous studies indicate that the mechanical state of stored maize kernel influences P. interpunctella development and that the broken kernels are the most suitable for its development and survival (Kaliyan et al., 2005; Mbata, 1990). However, in most of these studies, detailed data about developmental dynamics on different mechanical states of maize kernels
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were not given. Generally, there has been little investigation of P. interpunctella larval developmental dynamics, therefore our research was done to gather additional data on suitability of ground maize to development of P. interpunctella. Based on the endosperm and kernel composition, there exist six maize kernel types (Anonymous 2, 2008). Flint, dent and some of its semi-types are the most commonly grown kernel types in Europe and North America. The basic difference among these types of kernel is in the proportion of floury and horny endosperm, which differs among them (Anonymous 2, 2008). Flint kernels have high percentage of horny endosperm around the small soft center, while dent kernels have horny endosperm on the sides and the base of the kernel (Anonymous 2, 2008). According to the CIMMYT/IBPGR (1991) description, semi-flint maize kernels are flint kernels with a soft cup. Floury endosperm is softer and easier to break than horny endosperm (Babic et al., 2013). The type and ratio of endosperm in maize are directly connected to kernel hardness (Vieira Filho et al., 2015). Very few maize hybrids and kernel types have been tested for susceptibility to any storage insect pests. Harris and Green (1959) reported that damage caused by Sitophilus oryzae (L. 1763), was low on flint kernels, medium on semi flint kernels and the highest on dent varieties of maize. Our hypothesis was that kernel hardness significantly influences the life history of P. interpunctella, i.e., harder maize kernels would be less vulnerable to damage caused by P. interpunctella. Testing kernel hardness and continuous improving of kernel resistance to the attacks of storage insect pests could provide smaller losses in the quality and quantity of stored cereals in the future. Kernel hardness should be an important parameter when choosing maize hybrid for growing. It has been known that fecundity, development time and other biological parameters of P. interpunctella depend on the food source (Mohandass et al., 2007). The objective of our research was to investigate the influence of different mechanical states (whole, broken and ground kernels) and types (dent, semi flint and flint) of maize kernels to P. interpunctella life history. We wanted to determine whether P. interpunctella life history parameters (larval development and its dynamics, adult emergence, mean development duration and fecundity) depend on maize kernel state and type. Synergistic effects regarding type and state of kernels on P. interpunctella development history were also investigated. 2. Materials and methods 2.1. Maize kernels The experiment was carried out by using the following maize hybrids as nutrient mediums: NS 6130 (FAO 600), an experimental NS hybrid (FAO 600) and NS 1090 (FAO 170e190). All of the tested maize hybrids were in different type of kernel - dent, flint and semi-flint, respectively. Three mechanical states of kernels were used: whole undamaged kernels, mechanically broken kernels and ground kernels (whole grain corn flour). Maize hybrids were selections obtained from the Institute of Field and Vegetable Crops, Novi Sad, Republic of Serbia. The kernels were not treated with insecticides after the harvest or before setting up the experiment. Before starting the experiment, all of the used kernels were exposed to deep freezing (80 C), in order to eliminate possible presence of storage insect pests and parasites. 2.2. Insect cultures Plodia interpunctella cultures used in this research originated from a population reared for several years in The Laboratory for General and Applied Entomology, Faculty of Science, University of
Kragujevac, Serbia. Parental populations were reared in transparent plastic containers for mass rearing (1.2 L in volume), at chamber set at 28 ± 1 C, r.h. 60 ± 10% and 14:10 (L:D) photoperiod, on a standard laboratory diet for P. interpunctella (Silhacek and Miller, 1972). Moths in copuli were isolated from mass rearing containers and placed into oviposition jars, to collect one-day-old P. interpunctella eggs. Before the actual experiment, eggs were observed with a binocular microscope to eliminate those with obvious deformities. 2.3. Experimental design The experiment was set up as a randomized 3 3 4 block design type. We used three types of maize kernels (dent, semi flint and flint), in three different mechanical states. Each kernel type and state was repeated four times, with a total of 36 assays. The experiment was carried out by placing 100 g of mentioned kernel type and state into 0.25 L glass jars, in which 100 one-day-old P. interpunctella eggs were added. Jars were sealed with swab of cotton, coated with cotton cloth, for proper aeration. The experiment was carried out in environmental conditions described for the rearing of parental moth population. 2.4. Experimental procedure Ten days after setting up the experiment, larvae were collected from the hatched eggs. The examination started ten days after the beginning of the experiment, because 5e7 days old larvae were not easily noticeable, due to their very small size, light color and preference to hide inside the kernel. The head capsule width was measured for all collected larvae, using an ocular micrometer of binocular microscope. Based on the data obtained, different larval instars were distinguished (Allotey and Goswami, 1990) and the duration and dynamics of larval development period was determined. After the first examination, these actions were repeated every five days, until the last larva became a pupa. Once the emergence of the adults began, assays were checked once every 12 h and the number of the emerged adults and their gender was recorded. After that, newly emerged unmated adults from the same assay were immediately paired and each pair in copuli was isolated in a separate test tube. In order to obtain fecundity data, the number of eggs laid per female was recorded daily until the females died. The fecundity was defined as the total number of eggs laid after the mating. In the end of the experiment, the mean development duration (MDD) was calculated for each P. interpunctella adult, as the average time (in days), from the start of the experiment to each adult emergence. Based on the percentage of adult emergence and the mean values of MDD, the susceptibility index (Dobie, 1974) was calculated, according to the Howe's method (1971). 2.5. Statistical analysis Data were statistically analyzed using the IBM SPSS Statistics 21 software package (IBM, 2012). A two-way analysis of variance (ANOVA) was carried out to test the influence of the state and the type of kernels, as well as their synergistic effect on the larval development of P. interpunctella. Means of head capsule width among different state and type of kernel were compared using the multiple comparisons Tukey HSD test (P < 0.05). A one-way ANOVA was performed to test the influence of kernel state and type on the MDD and fecundity. Means of MDD and fecundity among different state and type of kernel were compared using the Dunnet T3 test (P < 0.05).
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3. Results 3.1. Larval development The results on duration and dynamics of larval development tested on three maize kernel states and types are presented in Tables 1e3. The fastest development and the highest increase in head capsule width were recorded between the 10th and 15th day of larval development, on all states and types of maize kernels. In this period, larvae doubled the width of their head capsule. Larvae reared on broken kernels reached the fifth instar five days earlier than on ground kernels and ten days earlier than those reared on whole kernels. Larval development was the shortest on ground kernels and it lasted for 30 days on all three kernel types. However, the number of individuals that finished the life cycle was the highest on broken kernels, although their larval development lasted for 35e40 days. The duration and dynamics of larval development differed among three tested maize kernel states and types (Table 4). The mechanical state and type of kernels as well as the synergistic effect between these two factors had influenced the larval development (Table 4). The mechanical state of kernels had the most significant influence. State of kernels had significant influence during almost the entire period of larval development, except in the period between 10th and 15th day (Table 4). Type of kernels, had statistically significant influence, although lower than the state of kernels, even during the 10th to 15th day period, up until 25th day of larval development (Table 4). The synergistic effect of state and type of kernel on P. interpunctella larval development also existed, especially during the first 15 days (Table 4).
3.2. Adult emergence and mean developmental duration The results on the mean number of emerged adults and mean developmental duration (MDD) are presented in Table 5. The highest mean number of emerged adults was recorded on broken kernels, while the lowest on whole ones. There were no statistically significant differences in the number of emerged adults among different kernel types in the state of broken and ground kernels (F2,9 ¼ 0.698, P ¼ 0.523; F2,9 ¼ 0.707, P ¼ 0.519, respectively). However, there were some statistically significant differences in number of emerged adults on whole kernels, but only between dent and semi-flint type (P ¼ 0.027). State of kernel showed high influence on the number of emerged adults. Significant differences
123
were recorded between number of emerged adults on whole and broken (P < 0.0005), as well as between whole and ground kernels (P < 0.0005). The shortest MDD have had moths in assays with broken dent kernels (34 d), while the longest MDD have had those reared on ground semi-flint kernels (47 d). The state of kernels showed statistically significant influence on P. interpunctella MDD, unlike the type of kernels (Table 5). Moths reared on broken dent kernels had significantly shorter MDD (34 d), compared to those reared on whole and ground dent kernels (38.5 d; 46 d; P ¼ 0.042; P < 0.0005, respectively). Similar and significant effects of kernel state on MDD were observed for semi-flint kernels. Moths reared on whole and broken semi-flint kernels had significantly shorter MDD (37.2 d, 38 d, respectively), compared to those reared on ground semi-flint kernels (47 d; P ¼ 0.003; P ¼ 0.001, respectively). There were no significant differences in MDD among different states of flint kernel type (F2,11 ¼ 3.521; P ¼ 0.074). 3.3. Susceptibility indices of different maize kernel state and type to infestation by P. interpunctella Susceptibility indices for the development of P. interpunctella on different types and states of maize kernels are given in Table 5. According to Mensah (1986), maize hybrids with susceptibility indices less than 2.5 are considered to be resistant to infestation by P. interpunctella. In our study, this includes whole kernels in the type of dent and flint, but not the semi-flint, which was medium resistant. The medium resistant kernels were those with values of susceptibility indices between 2.6 and 5. The kernels with susceptibility indices between 7.6 and 10.00 were deemed as susceptible to infestation by P. interpunctella. All types of broken kernels belong to this group (Table 5). Based on results of Dobbie index of susceptibility, all types of ground kernels were considered as moderately susceptible to infestation by P. interpunctella, with indices values between 5.1 and 7.5. The highest values of susceptibility index were for broken flint kernels (9.72), while the lowest were for whole dent kernels (1.81). Suitability of maize kernel is not influenced by the type of kernel, but only with the state of kernel (P < 0.0005) (Table 5). 3.4. Fecundity Results on the total number of mated adults and average fecundity are shown in Table 6. On average, fecundity was the
Table 1 Mean (±SE) larval head capsule widths (in mm), larval instars, comparison among instars and mean growth ratio of Plodia interpunctella reared on whole, broken and ground dent kernels. State of kernel
Number of days since the beginning of the experiment 10
15
20
25
30
35
40
H. w. (mm)a (±SE) Instar C. I. Ratio
0.193 (±0.006) I e
H. w. (mm)a (±SE) Instar C. I. Ratio
0.306 (±0.009) I e
Ground
H. w. (mm)a (±SE) Instar C. I. Ratio
0.21 (±0.007) I e
0.656 (±0.033) III III/II 1.7 0.908 (±0.009) V V20 d/II 1.63 0.59 (±0.011) III III-II 1.44
0.861 (±0.221) V V25 d/III 1.31 1.127 (±0.015) V V25 d/V20 d 1.24 0.91 (±0.006) V V25 d/III 1.54
1.081 (±0.048) V V30 d/V25 d 1.25 1.246 (±0.03) V V30 d/V25 d 1.105 1.04 (±0.022) V V30 d/V25 d 1.14
1.137 (±0.087) V V35 d/V30 d 1.05 1.252 (±0.06) V V35 d/V30 d 1.005 e
e
Broken
0.386 (±0.019) II II/I 2.0 0.555 (±0.01) II II-I 1.81 0.41 (±0.005) II II/I 1.95
e
e
Whole
e 1.3 (±0.06) V V40 d/V35 d 1.04 e
C. I. e Compared Instars. a H. W. (mm) e each datum is calculated based on the mean values of head capsule width (in mm) measured for all collected larvae in four replicates (for each state of dent kernel type).
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Table 2 Mean (±SE) larval head capsule widths (in mm), larval instars, comparison among instars and mean growth ratio of Plodia interpunctella reared on whole, broken and ground semi-flint kernels. State of kernel
Number of days since the beginning of the experiment 10
15
20
25
30
35
40
Whole
a
H. w. (mm) (±SE) Instar C. I. Ratio
0.143 (±0.018) I e
Broken
H. w. (mm)a (±SE) Instar C. I. Ratio
0.256 (±0.009) I e 0.23 (±0.008) I e
0.693 (±0.04) III III/II 1.925 0.972 (±0.015) V V20 d/III 1.5 0.66 (±0.09) III III/II 1.57
0.75 (±0.04) IV IV/III 1.08 1.056 (±0.023) V V25 d/V20 d 1.09 0.93 (±0.0007) V V25 d/III 1.4
1.09 (±0.198) V V30 d/IV 1.45 1.211 (±0.026) V V30 d/V25 d 1.15 1.05 (±0.012) V V30 d/V25 d 1.13
1.225 (±0.037) V V35 d/V30 d 0.97 1.325 (±0.03) V V35 d/V30 d 1.09 e
1.267 (±0.028) V V40 d/V35 d 1.03 1.4-V
H. w. (mm)a (±SE) Instar C. I. Ratio
0.36 (±0.031) II II/I 2.52 0.64 (±0.013) III III/I 2.5 0.42 (±0.005) II II/I 1.82
e
e
Ground
V40 d/V35 1.056 e
d
C. I. e Compared Instars. a H. W. (mm) e each datum is calculated based on the mean values of head capsule width (in mm) measured for all collected larvae in four replicates, for each state of semiflint kernel type.
Table 3 Mean (±SE) larval head capsule widths (in mm), larval instars, comparison among instars and mean growth ratio of Plodia interpunctella reared on whole, broken and ground flint kernels. State of kernel
Whole
Broken
Ground
Number of days since the beginning of the experiment 10
15
20
25
30
35
40
H. w. (mm)a (±SE) Instar C. I. Ratio
0.19 (±0.008) I e 0.321 (±0.009) I
0.75 (±0.036) IV IV/III 1.2 1.226 (±0.013) V
1.021 (±0.034) V V30 d/IV 1.36 1.248 (±0.03) V
1.105 (±0.062) V V35 d/V30 d 1.08 1.256 (±0.06) V
C. I. Ratio
e 0.23 (±0.008) I e
V25 d/V20 d 1.3 0.92 (±0.001) V V25 d/III 1.37
V30 d/V25 d 1.02 0.95 (±0.002) V V25 d/V20 d 1.03
V35 d/V30 1 e
e
H. w. (mm)a (±SE) Instar C. I. Ratio
0.626 (±0.03) III III/II 1.51 0.945 (±0.01) V V20 d/IV 1.26 0.67 (±0.009) III III/II 1.56
1.2-V
H. w. (mm)a (±SE) Instar
0.413 (±0.017) II II/I 2.17 0.747 (±0.014) IV IV-I 2.33 0.43 (±0.007) II II/I 1.87
d
e
V40 d/V35 1.08 e
d
e e
C. I. e Compared Instars. a H. W. (mm) e each datum is calculated based on the mean values of head capsule width (in mm) measured for all collected larvae in four replicates, for each state of flint kernel type.
Table 4 Statistical analysis of influence of different maize kernel states, types and their synergistic effect on differences in head capsule width of Plodia interpunctella larvae. Number of days since the beginning of the experiment
State of kernela
Type of kernela
Synergistic effectb
10
15
20
25
30
35
40
F ¼ 88.647 df ¼ 2,36 P < 0.0005* F ¼ 5.582 df ¼ 2,36 P ¼ 0.004* F ¼ 3.609 df ¼ 4,36 P ¼ 0.006*
F ¼ 0.979 df ¼ 2,36 P ¼ 0.376 F ¼ 6.270 df ¼ 2,36 P ¼ 0.002* F ¼ 22.889 df ¼ 4,36 P < 0.0005*
F ¼ 133.353 df ¼ 2,36 P < 0.0005* F ¼ 4.254 df ¼ 2,36 P ¼ 0.025* F ¼ 1.074 df ¼ 4,36 P ¼ 0.389
F ¼ 232.024 df ¼ 2,36 P < 0.0005* F ¼ 8.484 df ¼ 2,36 P ¼ 0.001* F ¼ 10.392 df ¼ 4,36 P < 0.0005*
F ¼ 9.910 df ¼ 2,36 P ¼ 0.001* F ¼ 0.802 df ¼ 2,36 P ¼ 0.459 F ¼ 0.906 df ¼ 4,36 P ¼ 0.475
F ¼ 12.885 df ¼ 2,36 P < 0.0005* F ¼ 0.043 df ¼ 2,36 P ¼ 0.958 F ¼ 1.522 df ¼ 4,36 P ¼ 0.224
F ¼ 3.846 df ¼ 2,36 P ¼ 0.034* F ¼ 1.871 df ¼ 2,36 P ¼ 0.173 F ¼ 3.957 df ¼ 4,36 P ¼ 0.012*
(a)Each datum is statistically analyzed based on the mean width of larval head capsule measured for all collected larvae in four and (b) eight replicates, each set up with 100 eggs. P values having asterisk (*) in superscript are significantly different by two-way ANOVA and Tukey HSD test at P < 0.05.
highest for moths reared on broken kernels, followed by those reared on ground and whole ones. The highest fecundity was recorded on broken dent, while the lowest on whole dent kernels. There were no statistically significant differences in fecundity among different kernel types in the state of whole and broken kernels (F2,7 ¼ 2.121, P ¼ 0.190; F2,127 ¼ 0.062, P ¼ 0.940,
respectively). However, there were some statistically significant differences in fecundity on ground kernels, among dent, semi-flint and flint type (P < 0.0005; P < 0.0005, P < 0.0005, respectively). When comparing fecundity among different states of one kernel type, there were some significant differences. Mean fecundity on broken and ground dent kernels were significantly higher than on
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125
Table 5 Mean number of emerged adults, mean developmental duration and mean susceptibility index (±SE) of Plodia interpunctella on different kernel states (whole, broken and ground) and types of maize. State of kernels
Maize kernel type
Mean number of emerged adults ± SE
Mean developmental duration ± SE
Mean susceptibility index ± SE
Whole
Dent Semi flint Flint Dent Semi flint Flint Dent Semi flint Flint
1.75 ± 0.25a1 4.25 ± 0.85b2 2.25 ± 0.25c 27.25 ± 3.84 28.25 ± 2.78 32 ± 2.12 18.75 ± 1.93 24.5 ± 5.33 18.5 ± 4.09
38.5 ± 0.64 a 37.2 ± 2.831 42.4 ± 3.53 34 ± 1.5 b 38 ± 2.061 35.7 ± 1.41 46 ± 0.82 c 47 ± 0.412 43.5 ± 0.64
1.81 3.69 1.94 9.67 8.87 9.72 6.34 6.68 6.54
Broken
Ground
± ± ± ± ± ± ± ± ±
0.041 (R)* 0.66 (MR) * 0.37 (R) * 0.447 (S) * 0.72 (S) * 0.34 (S) * 0.16 (MS) * 0.43 (MS) * 0.59 (MS) *
R e resistant; MR e medium resistant; S e susceptible; MS e medium susceptible (Mensah, 1986). Vertical mean values of number of emerged adults and MDD having different letter (a, b, c, for compared different states of kernel) or different number (1, 2, for compared different types of kernel) in superscript are statistically different by one-way ANOVA test and Dunnet T3 test at P < 0.05. Vertical values of mean susceptibility index among different state of one kernel type having asterisk (*) in superscript are statistically different by one-way ANOVA test and Bonferroni at P < 0.05.
Table 6 The total number of mated Plodia interpunctella females and their mean fecundity on different maize kernel states and types. Maize kernel type
Whole kernels Mated females
Dent Semi flint Flint Mean fecundity
4 4 2
Broken kernels Fecundity
Mated females
Range
Mean ± SE
22e44 33e154 40e95
27.75 ± 5.42b 81 ± 25.73a,b 67.5 ± 27.5a,b 57 ± 13.23
38 35 57
Ground kernels Fecundity
Mated females
Range
Mean ± SE
18e225 19e171 16e178
113.37 109.94 109.42 110.42
± ± ± ±
7.99a 7.04a 4.57a 3.58
12 23 17
Fecundity Range
Mean ± SE
96e170 43e92 65e95
114.33 ± 6.17a* 61.17 ± 2.33b* 79.76 ± 1.74b* 79.52 ± 3.41
Horizontal values having different letter (a, b, c) in superscript are statistically different by one-way ANOVA test and Dunnet T3 test at P < 0.05. Vertical values having asterisk (*) in superscript are statistically different by one-way ANOVA and Dunnet T3 test at P < 0.05.
whole ones (P < 0.0005, P < 0.0005, respectively). Highly significant differences were recorded between broken and ground kernels for both semi-flint and flint (P < 0.0005, P < 0.0005, respectively). There were no significant differences when comparing fecundity on broken and ground kernels to fecundity on whole kernels for semiflint (P ¼ 0.656; P ¼ 0.828, respectively) and flint (P ¼ 0.989; P ¼ 0.923, respectively) (Table 6). 4. Discussion Several studies have been conducted to determine the effect of maize variety on the development and survival of P. interpunctella, to identify different resistant varieties (Abdel-Rahman et al., 1968; Mbata, 1990). Results of our study have shown that mechanical state and type of kernels, as well as their synergistic effect, highly influences larval development, based on head capsule width measurements and survival of P. interpunctella adults. The mechanical state of kernels had a higher influence on larval development and number of emerged adults, succeeded by the type of kernels and synergy effect of kernel state and type. The data on the development time of individual instars of P. interpunctella is limited in the published literature (Mohandass et al., 2007). Results of our study have shown that feeding on broken kernels has led to the fastest development, the highest increase in head capsule width and the highest rate of survival of adults. This is in accordance with results of Mbata (1990) who reported that, when reared on broken maize kernels, P. interpunctella larvae usually developed significantly faster, compared to the development speed of those reared on whole maize kernels. LeCato (1976) found that cracked and ground kernels were more favorable for growth, development and production of P. interpunctella adult progeny. According to Kaliyan et al. (2005), a very low percentage
of larvae survived on whole kernels (7e28%). The results of our study are in accordance with these literature published data. Mbata (1990) and Kaliyan et al. (2005) suggested that the integrity of maize kernels is crucial for protection of stored maize, since whole kernels are much less susceptible to attack by P. interpunctella larvae. The results of our study confirm that whole kernels are the most resistant to infestation by P. interpunctella, unlike ground and broken ones which are medium susceptible or susceptible to infestation, respectively. The longest MDD was perceived with moths reared on ground kernels. This prolonged development has led to smaller number of emerged moths than we had expected based on the number of larvae registered during the head capsule measurements. Other authors have already confirmed negative correlation between duration of larval development and the number of emerged adults. Williams (1964) reported that mortality of pre-adult stages is usually higher in prolonged developmental period. Means of MDD reported here are in accordance with literature data: 28.4e35.3 days (Abdel-Rahman et al., 1968) and 34.5 days (Arbogast, 2007) on whole maize kernels; 25.9e38 days (Mbata, 1990) and 28.5 days (Imura and Sinha, 1986) on broken kernels; 28.05 days in ground maize (Allotey and Goswami, 1990). Fecundity was also significantly influenced by mechanical state of kernels since the highest fecundity was on broken and the lowest on whole kernels. Only a few studies reported values of fecundity of P. interpunctella reared on maize. Fecundity of moth population from farm-stored maize was 208.1 (Arbogast, 2007), while 174.2 on broken maize kernels (Allotey and Goswami, 1990). Lower values of average fecundity reported in our study could be explained by Nansen and Phillips (2003) findings. These authors showed that, when mated, females were prevented from directly coming into contact with the food
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source, oviposition was significantly reduced. Mbata (1990) also reported that the number of eggs laid on maize varieties was significantly higher than the number deposited on the glass (empty Petri dish). In our experiment, females were isolated and laid eggs in empty glass test tubes. Larval survival and fecundity were influenced by the type of kernels, especially by broken and ground ones. Influence of different types of kernel is mainly based on differences in kernel structure and hardness. This is confirmed by Abdel-Rahman et al. (1968) who also suggest that numerical differences in larval survival among different maize varieties may be due to difference in kernel hardness. The influence of type of kernel on life history parameters of P. interpunctella was especially obvious when comparing fecundity among different types of broken and ground kernels. Females reared on dent kernel type laid the largest mean number of eggs, both on broken and ground kernels, with statistical differences only on different types of ground kernels. Dent kernel type was the softest kernel type tested in our study. It contains higher percentage of floury endosperm, which is softer and easier to break (Babic et al., 2013). Easier consumption of dent kernels and lower energy cost for breaking the kernel pericarp, might lead to higher mean fecundity. However, the highest total number of mated females and number of laid eggs were recorded on broken flint kernels, the hardest kernel type tested in our study. This can be due to highest percentage of horny endosperm, which have higher proportion of protein matrix (Babi c et al., 2013). It is well known that population size and developmental dynamics of P. interpunctella depends on both nutritive quality and mechanical state of available food (Locatelli and Limonta, 1998). Data on mean fecundity of P. interpunctella reared on different types of broken and ground kernels are limited in the published literature. The only available data about dependence of P. interpunctella fecundity on whole maize kernels of different type were given by Abdel-Rahman et al. (1968). These authors found that differences in fecundity of moths reared on whole kernels of different maize varieties were not significant, which is in accordance with our results. Synergistic effects of kernel state and type showed statistically significant influence during the first 15 days of larval development. During the mentioned period, while examining jars in search for larvae to measure, we noticed that larvae primarily attack the part of the kernel where the germ is, while the pericarp was the least damaged. This confirms that pericarp presents a barrier to larval attacks, which was also reported by Abdel-Rahman et al. (1968), LeCato (1976) and Sallam (1999). Although the mandibles of larvae are strong, they have difficulties in breaking the greatly resistant maize pericarp (Locatelli and Limonta, 1998; Kaliyan et al., 2005). This is the reason why larval development was mostly influenced by state of kernels from the 20th day and why only 33 adults (out of 1200 eggs added at the beginning of the experiment) emerged on whole kernels. In recent studies, Limonta et al. (2013) tested susceptibility of different maize variants to P. interpunctella and showed that larval penetration into the kernel was influenced by maize embryo properties; mutant seeds lacking embryos were less damaged and therefore showed the lowest mean number of adult insects. Acknowledgements This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. We are thankful to Zeljko Milovac, PhD, for supplying us with maize kernels from Institute of Field and Vegetable Crops, Novi Sad, Serbia.
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